V 


BIOLOGY 

LIBRARY 

G 


VOL.  XXXVIII,  No.  449  MAY,  1904 

THE 

AMERICAN 
NATURALIST 


CONTENTS 

Page 

I.   The  Anatomy  of  the  North  American  Coniferales  together  with  Certain  Exotic 

Species  (continued.} PROFESSOR  D.  P.  PENHALLOW  331 

II.    Further  Instances  of  Malar  Division  .....    DR.  ALES  HRDLICZA  361 

in.    Studies  on  the  Plant  Cell— I DR.  BRADLEY  MOORE  DAVIS  367 

IV.  Notes  and  Literature:  General  Biology,  Plankton  of  the  Illinos  River,  Where  397 
did  Life  Begin  ?    Bermuda,  Morgan  on   Evolution   and   Adaptation  — 

Zoology,  Zoological  Investigations  in  the  Malay  Archipelago,  Davison's  399 

Anatomy  of  the  Cat,  Notes  —  Botany,  The  Journals,  Notes  .       .      .       .  402 

V-  Correspondence •  .      405 

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BIOLOGY 

The  American  Naturalist. 

ASSOCIATE   EDITORS  : 

J.  A.  ALLEN,  PH.D.,  American  Museum  of  Natural  History,  New  York. 
E.  A.  ANDREWS,  ¥u.T>.,fohns  Hopkins  University,  Baltimore. 
WILLIAM  S.  BAYLEY,  FH.D.,  Colby  University,  Waitrvill* 
DOUGLAS  H.  CAMPBELL,  PH.D.,  Stanford  University. 
J.  H.  COMSTOCK,  S.B.,  Cornell  University,  Ithaca. 
WILLIAM   M.  DAVIS,  M.E,,  Harvard  University,  Cambridge. 
ALES  HRDLICKA,  M.D.,   U.S.  National  Museum,  Washington. 
D.  S.  JORDAN,  LL.D.,  Stanford  University. 

CHARLES  A.  KOFOID,  PH.D.,   University  of  California,  Btrkelty. 
J,  G.  NEEDHAM,  PH.D.,  Lake  Forest  University. 
ARNOLD  E.  ORTMANN,  PH.D.,  Carnegie  Museum,  Pittsburg. 
D.  P.  PENHALLOW.D.SC..F.R.M.S.,  McGUl  University,  Montreal, 
H.  M.  RICHARDS,  S.D.,  Columbia  University,  New  York. 
W.  E.  RITTER,  PH.D.,  University  of  California,  Berkeley. 
ISRAEL  C.  RUSSELL,  LL.D.,  University  of  Michigan,  Ann  Arbor. 
ERWIN   F.  SMITH,  S.D.,  U.S.  Department  of  Agriculture,  Washington. 
LEONHARD    STEJNEGER,  LL.D.,  Smithsonian  Institution,  Washington, 
W.  TRELEASE,  S.D.,  Missouri  Botanical  Garden,  St.  Louis. 
HENRY  B.  WARD,  PH.D.,  University  of  Nebraska,  Lincoln. 
WILLIAM  M.  WHEELER,  PH.D.,  American  Museum  of  Natural  History, 
New  York. 

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-f 


>-^ « 4 


STUDIES  ON  THE   PLANT    CELL.— I. 

BRADLEY  MOORE  DAVIS. 

INTRODUCTION. 


is  of  papers  that  will  follow  one 
American  Naturalist.  They  will 
in  plant  cells  and  the  most 
histories,  largely  from  the  point  of 
tudent  of  developmental  processes, 
has  entirely  outrun  the  general 
several  botanical  text  books  and 
zoologists.  We  shall  attempt  to 
subject  in  its  present  state  with 
nt  papers  ;  but  this  is  not  to  be  an 
ire  that  is  already  very  large  and 
:d  far  more  satisfactorily  several 
passed  through  the  criticism  that 
y  active  botanical  investigation, 
^ason  to  be  proud  of  the  achieve- 
-esearch  upon  the  morphology  and 
r  much  of  the  best  work  of  recent 
'his  in  itself  has  been  a  great  stim- 
nese  brief  accounts  which  he  hopes 
:  to  a  clearer  understanding  of  the 
will  also  serve  to  contrast  the  pro- 
mts with  those  of  the  animal  cell 
in  several  foreign  works  and  in 
n  Development  and  Inheritance. 
lly  gratified  if  these  papers  should 
/ards  investigations  on  the  plant 

"cemriS!Tllfl!!Wr^ffl^^^B^  prevalent  among  botanists.  There 
is  a  tendency  to  regard  cell  studies  as  a  very  special  field  of 
botanical  research  with  elaborate  technique  which  the  average 

367 


The  American  Naturalist. 


BIOi.OGY 
LIBRARY 


ASSOCIATE   EDITORS: 

J.  A.  ALLEN,  PH.D.,  American  Museum  of  Natural  History,  New  York. 

E.  A.  ANDREWS,  PH.D.,/^«J  Hopkins  University,  Baltimore. 

WILLIAM  S.  BAYLEY,  FH.D.,  Colby  University,  mutrvili* 

DOUGLAS  H.  CAMPBELL,  PH.D.,  Stanford  University. 

J.  H.  COMSTOCK,  S.B.,  Cornell  University,  Ithaca. 

WILLIAM   M.  DAVIS,  M.E,,  Harvard  University,  Cambridge. 

ALES  HRDLICKA,  M.D.,  U.S.  National  Museum,  Washington. 

D.  S.  JORDAN,  LL.D.,  Stanford  University. 

CHARLES  A.  KOFOID,  PH.D.,   University  of  California,  Btrkelty. 

J,  G.  NEEDHAM,  PH.D.,  Lake  Forest  University. 

ARNOLD  E.  ORTMANN,  PH.D.,  Carnegie 

D.  P.  PENHALLOW.D.SC..F.R.M.S.,  MC&I 

H.  M.  RICHARDS,  S.D.,  Columbia  Universe 
W.  E.  RITTER,  PH.D.,  University  of  Califm 
ISRAEL  C.  RUSSELL,  LL.D.,  University  o 
ERWIN  F.  SMITH,  S.D.,  U.  S.  Department 
LEONHARD  STEJNEGER,  LL.D.,  Smith. 
W.  TRELEASE,  S.D.,  Missouri  Botanical  G. 
HENRY  B.  WARD,  PH.D.,  University  of  A 
WILLIAM  M.  WHEELER,  PH.D.,  Amer 
New  York. 

THE  AMERICAN  NATURALIST  is  an 
of  Natural  History,  and  will  aim  to  pres 
facts  and  discoveries  in  Anthropology 
Botany,  Paleontology,  Geology  and  Phj 
alogy  and  Petrography.  The  contents 
leading  original  articles  containing  acc< 
discoveries,  reports  of  scientific  expedi 
distinguished  naturalists,  or  critical  su 
line ;  and  in  addition  to  these  there  will 
points  of  interest,  editorial  comments  < 
day,  critical  reviews  of  recent  literatui 
gifts,  appointments,  retirements,  and  de 

All  naturalists  who  have  anything 
to  send  in  their  contributions,  but  the  < 
for  publication  only  that  which  is  of  tn 
same  time  written  so  as  to  be  intellignx 
to  the  general  scientific  reader. 

All  manuscripts,  books  for  revie\ 
sent  to  THE  AMERICAN  NATURALIST,  ( 

All  business  communications  sh 
publishers. 

Annual  subscription,  $4.00,  net,  in  adve 

Foreign  subscriptio 


EIBRARY 

IYCRSISTDF 


MBRHKY  FttOD 


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A 

. 

STUDIES  ON  THE    PLANT    CELL.— I. 

BRADLEY  MOORE  DAVIS. 

INTRODUCTION. 

THIS  is  the  first  of  a  series  of  papers  that  will  follow  one 
another  in  the  pages  of  the  American  Naturalist.  They  will 
describe  the  chief  structures  in  plant  cells  and  the  most 
important  events  in  their  life  histories,  largely  from  the  point  of 
view  of  the  morphologist  and  student  of  developmental  processes. 
Research  upon  the  plant  cell  has  entirely  outrun  the  general 
accounts  that  may  be  found  in  several  botanical  text  books  and 
in  certain  works  of  prominent  zoologists.  We  shall  attempt  to 
give  a  general  survey  of  the  subject  in  its  present  state  with 
references  to  the  most  important  papers  ;  but  this  is  not  to  be  an 
exhaustive  account  of  a  literature  that  is  already  very  large  and 
which  can  probably  be  treated  far  more  satisfactorily  several 
years  from  now  when  it  has  passed  through  the  criticism  that 
time  will  give  in  a  field  of  very  active  botanical  investigation. 

American  botanists  have  reason  to  be  proud  of  the  achieve- 
ments of  their  countrymen  in  research  upon  the  morphology  and 
physiology  of  the  plant  cell,  for  much  of  the  best  work  of  recent 
years  has  come  from  them.  This  in  itself  has  been  a  great  stim- 
ulus to  the  writer  to  prepare  these  brief  accounts  which  he  hopes 
will  assis.t  the  general  botanist  to  a  clearer  understanding  of  the 
progress  in  this  field.  They  will  also  serve  to  contrast  the  pro- 
toplasmic activities  among  plants  with  those  of  the  animal  cell 
which  has  been  so  well  treated  in  several  foreign  works  and  in 
English  by  Wilson's  The  Cell  in  Development  and  Inheritance. 

The  author  will  feel  especially  gratified  if  these  papers  should 
help  to  change  an  attitude  towards  investigations  on  the  plant 
cell  that  is  unfortunately  too  prevalent  among  botanists.  There 
is  a  tendency  to  regard  cell  studies  as  a  very  special  field  of 
botanical  research  with  elaborate  technique  which  the  average 

367 


368  THE  AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

botanist  cannot  be  expected  to  master.  Those  who  work  in  this 
field  are  considered  as  in  a  department  by  themselves  and  are 
labeled  cytologists  which  is  sometimes  given  as  an  excuse  for 
knowing  little  about  their  results.  Cell  studies  are  nothing  more 
than  morphological  and  physiological  investigations  which  are 
frequently  so  broad  as  to  break  the  mould  of  the  narrower  mor- 
phology and  physiology  of  former  years.  Cell  studies  must  be 
the  foundation  of  all  exhaustive  work  in  morphology  and  physi- 
ology. Indeed  among  the  lower  plants  they  constitute  almost  all 
there  is  to  morphology  and  will  determine  the  classification  and 
relationships  of  great  groups.  There  are  no  better  illustrations 
of  this  fact  than  the  effect  of  Prof.  Harper's  investigations  on 
the  ascus  and  sporangium  upon  Bref  eld's  theory  of  the  origin  of 
the  Ascomycetes.  And  again  the  results  of  several  investigators 
upon  the  multinucleate  gametes  found  among  the  Phycomycetes 
and  Ascomycetes  are  of  the  utmost  importance  to  a  correct 
understanding  of  the  phylogeny  of  these  groups.  When  students 
of  the  plant  cell  refuse  to  accept  the  stamp  of  cytologist  and 
insist  and  show  that  their  work  is  simply  fundamental  mor- 
phology and  physiology  we  shall  break  away  from  a  past  that 
should  be  outgrown. 

The  material  of  these  papers  will  be  treated  under  the  follow- 
ing heads. 

TABLE   OF  CONTENTS. 

Introduction. 

SECTION  I.     STRUCTURE  OF  THE  PLANT  CELL. 
i.   Protoplasmic  Contents.  ' 

(a)  The  Nucleus. 

(b)  The  Plastids. 

(c)  Cytoplasm. 

1.  Plasma  Membranes. 

2.  Trophoplasm. 

Coenocentra,  Nematoplasts,  Physodes. 

3.  Kinoplasm. 

Centrospheres,  Centrosomes,  Asters,  Filarplasm,  Ble- 
pharoplasts. 


No.  449-1  STUDIES   ON   THE  PLANT  CELL.  369 

2.  Non-Protoplasmic  Contents. 

(a)  Food  material  and  waste  products. 

(b)  Vacuoles. 

3.  The  Cell  Wall. 

SECTION  II.     THE  ACTIVITIES  OF  THE  PLANT  CELL. 

1.  Vegetative  Activities. 

2.  Cell  Division. 

(a)  The  Events  of  Nuclear  Division. 

1.  Direct  Division. 

2.  Indirect  Division  (Mitosis). 

Prophase,  Metaphase,  Anaphase,  Telophase. 

3.  The  Dynamics  of  Nuclear  Division. 

(b)  The  Segmentation  of  Protoplasm. 

1.  Cleavage  by  Constriction. 

2.  Cleavage  by  Cell  Plates. 

3.  Free  Cell  Formation. 

SECTION  III.     HIGHLY  SPECIALIZED  PLANT  CELLS  AND  THEIR 
PECULIARITIES. 

i.  The  Zoospore.  2.  The  Sperm.  3.  The  Egg.  4.  The 
Spore  Mother  Cell.  5.  The  Coenocyte.  6:  The  Coeno- 
gamete. 

SECTION  IV.  CELL  UNIONS  AND  NUCLEAR  FUSIONS  IN  PLANTS. 

SECTION  V.  CELL  ACTIVITIES  AT  CRITICAL  PERIODS  OF  ONTOG- 
ENY IN  PLANTS. 

i.  Garnet  ogenesis.  2.  Sporogenesis.  3.  Reduction  of 
Chromosomes.  4.  Apogamy.  5.  Apospory. 

SECTION  VI.  COMPARATIVE  MORPHOLOGY  AND  PHYSIOLOGY  OF 
THE  PLANT  CELL. 


370  THE  AMERICAN  NATURALIST.    [VOL.  XXXVI IK 

LITERATURE   ON    THE   PLANT   CELL. 

Reference  to  special  papers  will  be  given  by  the  authors  name 
and  the  date  of  publication  through  lists  presented  at  the  end  of 
every  section. 

There  is  no  comprehensive  treatise  devoted  to  the  plant  cell 
but  the  following  general  accounts  and  reviews  of  the  literature 
are  important. 

1.  Strasburger  in    the    Lehrbuch  der  Botanik    and   Pfeffer 
in  his   Physiology    of  Plants  present  the  best   general  accounts 
of  the  structure  and  activities  of  the  plant  cell. 

2.  Zimmerman  in  1893  and  '94  ("  Beihefte  zum  Botanischen 
Centralblatt  "  vol.  3   and  4),  reviewed  the  literature  on  the  plant 
cell  under  the  title  "  Sammel-Referate  aus  dem  Gesammtgebiete 
der  Zellenlehre "  and    in   1896  collected  the    literature  dealing 
with    the    nuclei  of   plants  in  a  book  entitled   Die  Morphologic 
und  Physiologic  des  pflanzliclien  Zellkernes,  Jena,  1896. 

3.  Dangeard  discusses  a  number  of  cytological  topics  in  the 
6th  series  of   Le  Botaniste  (1898)  with  especial  reference    to 
his  studies  on  the  Chlamydomonadineae. 

4.  Fischer,    Fixirung  Farbung  und  Bau    des  Protoplasmas 
Leipzig  1899,  presents  a  critique  of  the  methods  of  cytological 
research  and  the  justification  of  the  conclusions  based  thereon. 

5 .  The  most  recent  analysis  of  conspicuous  activities  of  the 
plant    cell    is  that    of    Strasburger    Ueber   Reductionstheilung, 
Spindelbildnng,    Centrosomen    und    Cilienbildner   im    Pflanzen- 
reich,  HistologiscJie  Beitriigc  VI,  I9OO.1 

SECTION  I.  STRUCTURE  OF  THE  PLANT  CELL. 

It  is  customary  to  apply  the  term  cell  in  Botany  not  alone  to 
the  protoplasmic  units  of  organization  but  also  to  the  enclosing 
wall  that  generally  surrounds  the  protoplasm.  Indeed  these 
walls  alone  when  entirely  emptied  of  protoplasm  in  specialized 

1  To  this  list  should  be  added  an  excellent  concise  review  by  Koernicke  entitled 
"Der  heutige  stand  der  pflanzlichen  zellforschung  "  Ber.  d.  dcut.  hot.  Gesell  21, 
(66),  1904.^  This  article  appeared  too  late  to  be  quoted  in  the  earlier  papers  of 
this  series. 


No.  449-1  STUDIES   ON   THE   PLANT  CELL.  371 

regions  of  the  plant,  e.  g.  vascular  and  certain  supporting  and 
tegumentary  tissues,  are  still  called  cells.  When  among  the 
lower  forms  and  at  certain  periods  in  the  life  history  of  many 
higher  plants  the  protoplasm  is  naked  (e.  g.  zoospores,  sperms, 
eggs,  etc.),  these  structures  are  cells  in  exactly  the  sense  used  by 
zoologists.  We  shall  consider  almost  entirely  the  protoplasmic 
portion  of  the  plant  structure  for  any  extended  treatment  of  the 
walls  would  lead  us  at  once  into  that  field  of  microscopic  anatomy 
termed  histology. 

i.     Protoplasmic    Contents. 

The  most  highly  differentiated  region  of  the  cell  is  the  nucleus,, 
a  structure  remarkably  uniform  in  organization  among  all  plants 
except  the  lowest  Algae  and  some  very  simple  Fungi.  These 
more  primitive  conditions  will  be  considered  in  Section.  VI. 
Besides  the  nucleus  there  are  present  plastids  in  all  groups 
except  the  Fungi.  Plastids  are  likewise  specialized  protoplasmic 
elements  although  much  simpler  in  structure  than  the  nucleus. 
Nuclei  and  plastids  lie  in  a  protoplasmic  matrix  called  the  cyto- 
plasm. Cytoplasm  is  more  variable  in  structure  and  activity 
than  any  other  region  of  the  cell.  Thus  three  forms  of  proto- 
plasm, nucleoplasm,  plastidplasm  and  cytoplasm  comprise  all  the 
living  material  of  the  cell  and  may  be  sharply  contrasted  with  the 
non-protoplasmic  contents,  mostly  food  material  and  waste  prod- 
ucts, which  will  be  considered  under  a  separate  head.  Definite 
masses  of  nucleate  protoplasm,  with  or  without  plastids  are 
termed  protoplasts  and  such  are  either  unicellular  organisms 
themselves  or  units  of  a  multicellular  structure. 

(a)     The  Nucleus. 

The  nucleus  is  bounded  by  a  delicate  membrane  that  is 
probably  largely  or  wholly  a  modification  of  the  surrounding  cyto- 
plasm. The  nucleoplasm  very  rarely  completely  fills  the  nuclear 
membrane,  the  remaining  space  being  occupied  by  a  fluid  known 
as  the  nuclear  sap.  The  elements  in  the  resting  nucleus  consist 
chiefly  -of  material  that  takes  the  form  of  a  net  work  so  that  the 


372 


THE  AMERICAN  NATURALIST.  [VOL.  XXXVI II. 


effect  is  that  of  a  much  coiled  and  twisted  thread  whose  loops  are 
united  at  intervals  to  form  large  and  small  meshes.  The  ground 
substance  of  this  thread  is  called  linin  and  imbedded  in  it  as  in 
a  matrix  are  deeply  staining  granules  of  chromatin.  Chromatin 
is  regarded  as  the  most  important  substance  in  the  nucleus, 
chiefly  because  of  its  behavior  during  nuclear  division,  and  in 
critical  periods  of  the  life  history  of  organisms  as  at  sporogen- 
esis,  gametogenesis  and  fertilization  (to  be  described  in  Section 
V).  Just  before  nuclear  division  the  chromatin  becomes  organ- 
ized into  bodies  named  chromosomes  which  are  remarkably  uni- 
form in  number  and  definite  in  shape  for  each  tissue  and  period 
of  the  plant's  life.  They  will  be  discussed  under  "  The  Events 
of  Nuclear  Division  "  (Section  II),  and  in  Sections  IV  and  V. 


FIG.  i. —  The  resting  nucleus.  «,  Embryo  sac  of  lily  with  linin  thread  and  two  nucleoli. 
6,  Root  of  onion  large  nucleolus.  c,  Tetraspore  of  Corallina  showing  large  chro- 
matin body  and  small  nucleolus.  d,  Spirogyra  with  central  body  containing  chroma- 
tin,  e,  Chromatin  on  linin  net  work  from  egg  of  pine.  After  Mitzkewitsch  and 
Chamberlain. 

In  the  meshes  of  the  linin  network  or  lying  freely  in  the 
nuclear  sap  may  be  found  one  or  more  bodies,  generally  globular 
in  form,  called  nucleoli.  (See  Fig.  i  a  and  Fig.  i  b}.  The 
nucleolus  is  generally  regarded  as  a  secretion  of  the  nucleus  and 
it  is  quite  certain  that  its  substance  is  utilized  just  previous  to 
and  during  the  period  of  nuclear  division  when  the  spindle  is 
formed.  (Strasburger  '95  and  :  oo,  p.  125,  and  from  the  work  of 
•others).  The  structure  is  not  always  homogeneous  but  may 
-show  in  the  interior  small  vesicles  or  areas  of  a  different  con- 
sistency from  the  periphery.  There  is  often  present  also  a 
rather  thick  outer  shell  or  membrane.  Sometimes  the  chromatin 
in  the  nucleus  may  be  gathered  into  a  globular  body  that  resem- 
bles superficially  a  nucleolus.  Such  chromatin  bodies  are  gen- 


No.  449.]  STUDIES  ON   JTfE    PLANT  CELL.  373 

erally  transitory  as  in  Corallina,  Davis  '98,  where  the  structure 
(Fig.  i  c)  is  only  found  in  the  young  daughter  nucleus  and  later 
fragments  into  many  smaller  bodies.  In  Spirogyra  however 
(Moll  '94,  Mitzkewitsch  '98,  Van  Wisselingh  :  oo,  '02)  the 
chromatin  is  supposed  to  be  always  in  a  globular  mass  mixed  with 
nucleolar  substance  and  recalls  the  conditions  in  certain  Protozoa. 
These  chromatic  structures  however  should  never  be  confused 
with  nucleoli,  whose  substance  is  different  and  which  are  not 
permanent  in  the  cell,  since  they  may  disappear  before  or  during 
nuclear  division  and  be  formed  de  novo  in  each  daughter  nucleus. 

The  substance  of  the  nucleolus  is  not  well  understood.  It  is 
frequently  impossible  to  distinguish  it  from  chromatin  except 
when  favorably  situated  in  the  cell  and  there  is  much  evidence 
that  it  is  closely  related  to  that  substance.  In  large  nuclei  of 
higher  plants  the  chromatin  is  sometimes  gathered  into  globular 
bodies  without  apparent  relation  to  a  linin  thread  and  these  are 
readily  mistaken  for  nucleoli  and  have  been  called  such,  but  this 
loose  usage  of  the  term  should  be  avoided.  And  true  nucleoli 
may  be  so  closely  associated  with  the  linin  net  work  as  to  have 
the  appearance  of  chromatin.  Some  of  these  conditions  have 
been  especially  described  by  Cavara,  '98.  Chamberlain,  '99,  has 
made  a  study  of  the  egg  nucleus  of  the  Pine  where  masses  of 
chromatin  may  take  very  irregular  forms  on  the  linin  threads 
(Fig.  i  e]  and  sometimes  resemble  small  nucleoli.  But  such 
conditions  should  always  be  sharply  distinguished  from  true 
nucleoli  which  are  often  caught  in  the  meshes  of  the  linin  net 
work  and  appear  to  be  a  part  of  it  when  in  reality  there  are  no 
organic  attachments.  It  is  certain  that  nucleoli  are  of  secondary 
importance  in  the  cell  and  probably  by-products  of  the  general 
constructive  activities  of  the  nucleus.  In  which  case  they  may 
be  secretions,  perhaps  closely  related  to  chromatin,  or  even  direct 
transformations  of  this  substance.  It  is  well  known  that  the 
nucleus  has  wonderful  constructive  powers,  when  the  amount  of 
chromatin  and  other  nuclear  substances  may  be  immensely 
increased,  facts  that  are  especially  well  illustrated  at  reproductive 
periods  of  the  plant's  life  as  during  sporogenesis  and  garnet o- 
genesis.  • 

Chromatin  is  the  only  substance  in  the  nucleus  that  is  constant 


374  THE  AMERICAN  NATURALIST.   [VOL.  XXXVI II. 

in  its  presence  throughout  all  periods  in  every  cell's  history. 
It  passes  on  from  cell  to  cell  through  the  mechanism  of  nuclear 
division  without  interruption.  There  are  periods  of  cell  history 
when  the  nucleus  consists  only  of  chromosomes  as  in  the  stages 
of  nuclear  division  called  mataphase  and  anaphase.  The  other 
structures  of  the  nucleus  have  their  relation  to  definite  condi- 
tions that  are  in  part  understood.  The  nuclear  membrane 
probably  results  from  the  reaction  of  the  cytoplasm  to  the  secre- 
tion of  nuclear  sap  among  the  chromosomes  (Lawson,  -.03  a). 
It  would  then  be  strictly  cytoplasmic  in  character  and  similar  to 
the  plasma  membranes  around  vacuoles.  Nucleoli  must  be 
regarded  as  temporary  structures  since  they  generally  disappear 
during  nuclear  division  either  dissolving  or  else  passing  out  into 
the  cytoplasm  where  they  may  remain  for  long  periods  as  deeply 
staining  globules  (extra  nuclear  nucleoli).  Linin  is  believed  to 
be  derived  from  chromatin  and  in  its  turn  may  be  transformed 
into  the  substance  of  spindle  fibers,  which  are  cytoplasmic,  so 
that  chemically  it  holds  a  position  somewhat  intermediate  between 
chromatin  and  cytoplasm.  It  seems  established  that  the  linin 
net  work  is  a  temporary  structure  related  to  the  activities  of 
chromatin. 

(b)     The  Plastids. 

These  very  interesting  structures,  characteristic  of  plant  cells, 
have  not  received  the  degree  of  attention  that  they  deserve 
and  much  valuable  work  may  be  done  in  the  detailed  study  of 
their  protoplasmic  structure  and  activities  at  various  periods  of 
ontogeny  especially  through  the  series  of  changes  that  are 
presented  during  developmental  processes. 

The  primitive  types  of  plastids  are  relatively  large  structures, 
often  solitary  in  the  cells,  and  generally  of  complex  form. 
These  are  called  chromatophores  and  are  characteristic  of  many 
algae  especially  among  the  lower  groups  but  are  not  found  above 
the  thallophytes  (Anthoceros  and  Selaginella  excepted). 

The  chromatophores  of  the  simplest  algae  are  replaced  in  most 
of  the  higher  types  of  these  thallophytes  and  in  all  groups 
above  by  very  much  smaller  structures,  generally  discoid  in 


No.  449-]  STUDIES   OA    THE   PLANT  CELL.  375 

form,  which  are  called  chloroplasts  when  green,  chromoplasts 
when  the  color  is  other  than  green  or  leucoplasts  if  colorless. 
These  plastids  are  without  doubt  derived  from  the  more  primitive 
chromatophores. 

The  colors  of  chromatophores  are  various.  They  are  believed 
always  to  contain  some  chlorophyll  but  this  green  is  frequently  so 
completely  masked  by  other  pigments  that  its  presence  can  only 
be  determined  when  the  additional  coloring  matters  have  been 
extracted.  Chloroplasts  are  universally  green  except  when  they 
may  be  changing  into  chromoplasts.  Chromoplasts  generally 
take  their  tint  from  the  predominance  of  other  strong  pigments 
in  addition  to  chlorophyll  as  phycoerythrin  in  the  red  and  phyco- 
phsein  in  the  brown  algae.  But  chromoplasts  may  be  derived 
from  chloroplasts  whose  green  has  largely  or  wholly  disap- 
peared leaving  other  pigments  present  as  the  yellow,  xanthophyll, 
or  the  orange  red,  carotin. 

The  remaining  plastids,  leucoplasts,  are  devoid  of  color  and 
are  found  in  embryonic  regions  such  as  eggs,  growing  points, 
and  in  the  various  tissues  of  seeds,  underground  organs  and 
other  structures  where  the  cells  are  largely  or  wholly  removed 
from  sunlight.  The  leucoplasts  may  become  green  upon  expo- 
sure to  light  thus  changing  into  chloroplasts.  They  are  respon- 
sible for  the  secretion  of  reserve  starch  in  many  structures  (e.  g. 
potato)  and  in  consequence  have  been  called  ^myloplasts. 

Leucoplasts,  chloroplasts  and  chromoplasts  are  morphologically 
the  same  structures.  It  is  well  known  that  they  may  pass  one 
into  the  other  in  the  order  indicated  and  that  chloroplasts  and 
chromoplasts  may  lose  their  color  and  become  leucoplasts.  It  is 
generally  believed  that  plastids  are  not  formed  de  novo.  They 
divide  by  constriction  and  thus  multiplying  are  passed  on  from 
cell  to  cell  and  it  is  believed  from  generation  to  generation. 
They  are  therefore  usually  ranked  as  permanent  organs  of  the 
cell.  However,  it  is  but  fair  to  call  attention  to  the  fact  that 
there  are  some  serious  difficulties  in  the  way  of  a  complete 
acceptation  of  these  views. 

The  protoplasmic  structure  of  the  plastids  of  higher  plants 
is  rather  simple  while  that  of  the  chromatophores  in  algae  is 
more  complex  since  they  contain  a  special  organ  termed  the 


376  THE  AMERICAN  NATURALIST.   [VOL.  XXXVIIL 

pyrenoid.  The  detailed  structure  of  chromatophores  was  first 
described  by  Schmitz  ('82)  and  of  plastids  by  Meyer  ('83). 
The  most  complete  study  of  plastids  however  is  that  of  Schimper 
('85).  The  body  of  the  plastid  is  always  denser  than  the  sur- 
rounding cytoplasm.  It  has  a  porous  structure  that  is  only 
visible  under  high  magnification  and  there  are  sometimes  present 
very  delicate  fibrils.  The  coloring  matter,  oily  in  consistency, 
is  held  in  the  pores  as  minute  globules.  The  plastid  may 
therefore  be  compared  to  a  very  fine-textured  sponge  saturated 
with  pigment.  All  of  the  coloring  matter  of  the  plastid  may 
be  readily  extracted  with  alcohol  leaving  the  colorless  proteid 
matrix. 

The  pigments  of  plastids  are  then  in  the  nature  of  secretions 
held  in  these  specialized  regions  of  protoplasm.  Chlorophyll  is 
the  principal  substance  and,  as  has  before  been  said,  is  almost 
always  present,  but  the  amount  is  sometimes  so  small  that  its 
green  is  completely  hidden  by  the  color  of  other  pigments. 
Chlorophyll  itself  contains  greater  or  less  amounts  of  two  other 
coloring  matters  that  may  be  readily  separated  from  the  pure 
green,  a  yellow  xanthophyll  and  an  orange  red  carotin,  both 
substances  closely  related  to  chlorophyll.  The  other  pigments, 
characteristic  of  the  chromatophores  in  some  groups  of  algae, 
are  however  quite  distinct  from  chlorophyll.  There  is  phycocyan, 
found  in  the  blue*  green  algae  (Cyanophyceae),  phycophaein  and 
phycoxanthin,  characteristic  of  the  brown  (Phaeophyceae)  and 
phycoerythrin  of  the  red  (Rhodophyceae). 

Chloroplasts  are  found  almost  universally  in  green  plants 
above  the  Thallophytes  and  are  also  present  in  the  large  group 
of  algae  the  Siphonales  and  in  the  Charales.  They  are  some- 
times formed  very  numerously  in  the  cell,  reproducing  rapidly 
by  fission  (see  Fig.  2  a  2,  3)  and  lie  in  the  layer  of  protoplasm 
just  inside  of  the  plasma  membrane.  They  are  sensitive  to  light 
and  readily  shift  their  position  in  the  cell.  Strong  illumination 
results  in  their  retreat  from  exposed  positions  to  the  sidewalls 
and  bottom  of  the  cell  where  the  light  is  less  intense.  If  the 
illumination  be  weak  they  may  all  gather  on  the  side  most  favor- 
able for  the  reception  of  light.  These  facts  are  well  illustrated 
by  the  behavior  of  the  plastids  in  some  of  the  Siphonales  (e.  g. 


No.  449.] 


STUDIES   ON  THE  PLANT  CELL. 


377 


Botrydium),  in  the  Rhodophyceae  (e.  g.  Polysiphonia)  and  also 
in  the  palisade  cells  of  leaves.  Chloroplasts  after  exposure  to 
light  generally  contain  starch  but  in  some  plants  this  substance 
is  never  formed  (e.  g.  Vaucheria,  Fig.  2  A  i),  the  nrsFvrsible 
products  of  photosynthesis  being  other  substances  more  of  the 
nature  of  oil.  It  is  not  known  whether  the  starch  grain  in  the 


PIG.  2. —  Plastids.  a,  Chloroplasts:  i  Vaucheria,  with  oil  globules;  2  Bryopsis ;  3 
moss  (Funaria),  in  division  and  containing  starch  grains  ;  4  Oxalis,  with  a  grain  of 
starch,  b,  Chromoplasts :  i  Tropaeolum,  epidermal  cell  from  calyx;  2  Fucus,  3 
Callithamnion.  c,  Chromatophores  :  i  Spirogyra,  with  pyrenoids  (/)  and  caryoicls 
(c);  2  Hydrodictyon,  pyreuoid  forming  starch;  3  Nemalion;  4  Anthoceros,  in  divi- 
sion and  containing  starch,  d,  Leucoplasts :  i  Ph.ijus,  pUstid  and  starch  grain  at 
the  side  of  the  nucleus  ;  2  Iris,  from  root  and  containing  oil  globules  ;  3  Iris,  in 
deeper  cells  of  root,  with  starch  grains.  After  Meyer,  Strasburger,  P.lla,  1  imber- 
l.ike  and  Schimper. 

chloroplast  results  from  the  direct  change  of  some  of  the  pro- 
teid  substance  or  whether  it  is  a  secretion.  The  conditions 
are  somewhat  different  when  pyrenoids  are  present  in  a  chro- 
matophore  as  will  be  described  presently. 

The   Chloroplasts  of  higher   plants  may   change   color  under 
various  conditions  and  become  chromoplasts.     Some  of  the  best 


378  THE  AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

examples  are  found  in  the  colored  cells  of  certain  floral  parts 
and  fruits  (Fig.  2,  b  i).  These  pigments  are  generally  either 
xanthophyll  (yellowish)  or  carotin  (orange  red).  Chloroplasts 
may  also  turn  brown  especially  in  older  cells  that  are  losing  their 
contents.  The  colors  of  some  leaves  and  flower  parts  are  due 
not  to  the  plastids  but  to  substances  dissolved  or  otherwise  held 
in  the  cell  sap  of  the  vacuoles.  The  brilliant  coloration  of 
autumn  foliage  is  of  this  character  as  well  as  some  of  the  tints 
of  petals,  hairs  and  other  structures.  The  chromatophores  of 
the  higher  brown  Algae  (Phaeophyceae)  and  most  of  the  red 
(Rhodophyceae)  have  the  discoid  form  characteristic  of  chloro- 
plasts  (Fig.  2  b  2,  3).  They  might  be  called  phasoplasts  and 
rhodoplasts  if  one  wished  to  classify  plastids  according  to  their 
color. 

The  structure  of  chromatophores  is  frequently  complicated  by 
the  presence  of  pyrenoids  which  may  be  quite  numerous  in  the 
body.  These  structures  are  denser  regions  of  the  chromatophore 
with  a  definite  boundary.  They  are  proteid  in  character  and 
are  known  to  vary  in  size  with  nutritive  conditions  and  may 
completely  disappear  if  the  cell  is  starved.  They  have  been 
regarded  as  masses  of  reserve  oroteid  material  but  certain  func- 
tions of  great  importance  are  also  associated  with  them.  The 
arrangement  of  starch  grains  in  the  chromatophores  of  many 
algae  is  clearly  around  the  pyrenoids  as  centers.  For  this  reason 
they  have  been  called  amylum  centers.  Timberlake  (:oi)  has 
recently  shown  in  Hydrodictyon  that  segments  are  split  off 
from  the  pyrenoids  (see  Fig.  2,  c  2)  and  changed  directly  into 
starch  grains  which  naturally  lie  for  a  time  close  to  the  source 
of  their  formation  and  only  later  become  distributed  throughout 
the  chromatophore.  It  is  probable  that  similar  conditions  will 
be  found  in  other  algae  (Conjugales,  Protococcales,  etc.)  and  we 
may  soon  have  a  much  clearer  understanding  of  the  pyrenoid. 
The  indications  are  that  the  pyrenoid  will  prove  to  be  a  region 
of  the  chromatophore  differentiated  as  a  metabolic  center,  more 
or  less  prominent  according  to  conditions  of  nutrition,  and  that 
its  most  conspicuous  activity  is  the  formation  of  starch  by  the 
-direct  transformation  of  portions  of  its  substance. 

Some    other    structures    besides    the    pyrenoids    have    been 


No.  449.]  STUDIES   ON   THE  PLANT  CELL.  379 

described  by  Palla  ('94)  in  the  chromatophores  of  several  of  the 
Conjugates  and  have  been  named  caryoids.  Caryoids  (Fig.  2, 
c  i)  are  smaller  and  more  numerous  than  pyrenoids  and  are 
distributed  irregularly  in  the  chromatophore  but  chiefly  "along 
the  edge.  Their  function  is  not  known. 

The  leucoplasts  complete  the  list  of  plastid  structures.  They 
are  colorless  and  may  be  found  in  underground  or  other  portions 
of  the  plant  removed  from  light  or  where  there  is  little  or  no 
photosynthetic  activities  as  in  embryo  sacs,  seeds,  growing  points, 
etc.  They  become  impregnated  with  chlorophyll  under  condi- 
tions suitable  for  photosynthesis  thus  changing  into  chloro- 
plasts.  An  important  function  of  the  leucoplast  is  the  forma- 
tion of  reserve  starch  in  various  parts  of  the  plant.  The  more 
recent  investigations  of  this  process  (Meyer,  '95,  Salter,  '98) 
claim  tfyat  it  is  in  the  nature  of  a  secretion  within  the  substance 
of  the  leucoplast.  This  view  is  opposed  to  the  older  conceptions 
{Schimper,  '81,  Eberdt,  '91),  which  regarded  the  starch  grain  as 
formed  by  the  direct  change  of  proteid  material  in  the  plastid. 
In  view  of  Timberlake's  (  :  01)  studies  on  the  pyrenoid  of  Hydro- 
dictyon  we  may  well  hesitate  to  fully  accept  the  views  of  Meyer 
and  Salter  and  ask  for  further  investigations  of  this  very  difficult 
subject.  In  addition  to  starch  leucoplasts  may  contain  proteid 
crystals  and  oil  globules. 

The  reproduction  of  plastids  and  their  evolutionary  history 
in  ontogeny  and  phylogeny  offers  a  very  attractive  field  for 
research.  It  is  well  known  that  plastids  multiply  by  fission  and 
it  is  generally  believed  that  they  never  arise  de  novo  but  are 
passed  from  generation  to  generation  as  permanent  organs  of 
the  cell.  The  process  of  division  may  be  very  favorably  studied 
in  the  spore  mother-cell  of  Anthoceros  (Fig.  2,  c  4).  The  fission 
begins  (Davis,  '99)  by  a  constriction  at  the  surface  as  though 
the  bounding  membrane  of  cytoplasm  exerted  pressure  upon  an 
elongating  structure.  There  is  no  evidence  that  the  interior  of 
the  chloroplast  undergoes  any  changes  that  could  assist  the 
process  further  than  a  possible  tendency  of  the  two  separating 
portions  to  gather  their  substance  together  as  division  proceeds. 
The  conditions  suggest  that  the  division  is  a  mechanical  separa- 
tion of  material  too  bulky  for  the  best  advantages  of  the  cell, 


3  8o  THE   AMERICAN  NA  TURAL1ST.   [VOL.  XXXV  III. 

for  the  proper  balance  of  protoplasmic  elements  in  narrow 
confines,  a  division  prompted  by  the  activities  of  the  cytoplasm 
rather  than  emanating  from  within  the  plastid. 

The  view  of  the  permanence  of  the  plastid  as  a  cell  organ  has 
received  its  strongest  support  from  the  classical  work  of 
Schimper  ('85).  We  are  not  prepared  to  deny  it  and  to  assert 
that  the  plastid  may  arise  de  novo.  Yet  those  who  study  the 
cells  of  embryonic  tissues  and  reproductive  phases  know  that  it 
is  extremely  difficult  to  follow  the  plastids  and  that  these 
structures  require  other  than  the  usual  methods  of  cell  research 
to  establish  their  presence.  Several  writers  (Eberdt,  Dangeard, 
Husekand  others)  have  expressed  their  belief  that  plastids  may 
arise  de  novo  but  no  one  has  thoroughly  traced  the  appearance 
or  disappearance  of  these  structures  in  any  cells. 

The  plastid  in  phylogeny  has  never  received  the  attention  that 
it  deserves.  Beginning  with  the  conditions  among  the  Cyano- 
phyceae  and  the  lowest  Chlorophyceae  (which  will  be  further 
discussed  in  Section  VI)  we  find  the  pigment  distributed  so 
generally  throughout  the  cell  that  it  is  doubtful  if  the  term 
chromatophore  should  ever  be  applied  to  regions  so  indefinite  in 
outline.  Above  these  groups  the  pigment  is  confined  to  propor- 
tionally smaller  areas  in  the  cytoplasm  and  these  become 
chromatophores  when  their  form  is  clear.  The  primitive  chro- 
matophores  were  solitary  and  filled  a  large  part  of  the  cell. 
The  pyrenoids  arose  in  the  chromatophores  probably  as  the 
result  of  the  influence  of  metabolic  centers  upon  the  protoplasm. 
It  is  scarcely  possible  that  a  large  chromatophore  should  be 
absolutely  homogeneous  throughout ;  there  would  develop  one 
or  more  centers  of  metabolic  activity  and  such  would  exert  some 
influence  on  the  form  of  the  protoplasm. 

But  the  large  single  chromatophore  does  not  seem  to  be  the 
form  best  adapted  to  the  work  of  a  cell  perhaps,  if  for  no  other 
reason,  because  it  requires  a  mechanical  adjustment  of  other 
cell  organs  to  itself  and  would  interfere  with  the  quick  circula- 
tion of  material  and  the  general  balance  of  cell  activities. 
It  seems  possible  that  mechanical  difficulties  may  have  led  to 
the  division  of  large  chromatophores  and  the  substitution  of 
numerous  small  plastids.  This  change  was  instituted  in  the 


No.  449.]  STUDIES   ON  THE  PLANT  CELL.  381 

higher  members  of  the  Phaeophyceae  and  Rhodophyceae  and  in 
the  Siphonales,  Charales,  Cladophoraceae  and  some  smaller 
groups  of  the  Chlorophyceae.  The  Conjugales  whose  chromato- 
phores  are  especially  elaborate  have  cells  essentially  solitary  in 
their  life  habits  and  with  a  very  remarkable  adjustment  of  the 
cell  organs  to  one  another  to  give  almost  perfect  symmetry. 
With  the  splitting  up  of  the  chromatophore  came  the  loss  of  the 
pyrenoid  and  the  final  result  was  the  compact  plastid  so  charac- 
teristic of  plants  above  the  thallophytes. 

I 

(c)     Cytoplasm. 

There  is  no  region  of  the  plant  cell  that  maintains  such  varied 
relations  to  its  environment  and  performs  so  many  visible 
activities  as  the  cytoplasm.  For  this  reason  the  accounts  of  its 
structure  and  behavior  have  been  diverse  and  there  has  developed 
a  nomenclature  of  its  parts  that  is  confusing  and  somewhat 
difficult  to  harmonize. 

Strasburger  has  for  many  years  (since  1892)  employed  the 
term  kinoplasm  to  distinguish  an  active  portion  of  the  cytoplasm 
(concerned  with  the  formation  of  spindle  fibers  and  other 
fibrillae,  centrospheres,  centrosomes,  cilia,  plasma  membranes, 
etc.)  from  more  passive  nutritive  regions  which  he  called  tropho- 
plasm.  Kinoplasm  corresponds  closely  to  the  archoplasm  of 
the  animal  cell  (Boveri,  1888).  This  classification  has  been 
criticised  especially  by  Pfeffer  ( :  oo)  on  the  ground  that  it 
employed  names  signifying  physiological  differences  when  the 
distinctions  as  far  as  we  know  are  those  of  morphology  alone. 
However  the  physiological  behavior  of  kinoplasm  and  tropho- 
plasm  becomes  very  real  to  anyone  who  studies  extensively  cell 
activities  and  the  morphological  characters  serve  to  emphasize 
these  peculiarities.  The  truth  seems  to  be  that  cell  studies 
cannot  be  pursued  from  the  standpoint  of  physiology  or  mor- 
phology alone  but  must  combine  these  attitudes.  And  in  the 
union  it  is  hardly  possible  or  perhaps  desirable  to  construct 
a  terminology  with  strict  regard  to  either  field  of  study.  We 
shall  use  the  terms  kinoplasm  and  trophoplasm  grouping  the 
various  cytoplasmic  structures  under  these  heads. 


382  THE   AMERICAN  NA  TURALIST.  [VoL.  XXXV  III. 

Cytoplasm  has  surface  contact  with  three  conditions  and  in 
each  case  there  is  present  a  delicate  plasma  membrane,  colorless 
and  very  finely  granular,  which  is  very' different  in  structure  from 
the  cytoplasm  within.  The  first  of  these  three  membranes  is 
the  outer  plasma  membrane,  which  bounding  the  protoplast,  is 
consequently  just  inside  the  cell  wall.  This  membrane  is  called 
the  "  hautschicht  "  by  the  German  botanists,  a  word  for  which 
we  have  no  exact  equivalent,  the  term  ectoplast  more  nearly 
expressing  the  meaning  than  any  other  but  for  several  reasons 
not  being  very  satisfactory.  Since  this  outer  plasma  membrane 
lies  against  a  moist  cell  wall  it  is  virtually  surrounded  by  a  film 
of  water.  The  functions  of  the  cell  wall  in  land  plants  and  its 
developmental  history  indicate  a  close  relation  to  the  demands 
of  the  outer  plasma  membrane  for  a  fairly  uniform  environment 
of  moisture,  a  matter  which  will  be  discussed  in  the  last  section 
of  these  papers. 

The  second  form  of  plasma  membrane  surrounds  the  water 
vacuoles  in  the  cell.  It  is  very  common  for  the  plant  cell  to 
have  a  single  large  central  vacuole  containing  the  cell  sap  and 
the  membrane  around  this  was  named  the  tonoplast  by  DeVries 
in  1885.  DeVries  believed  that  this  vacuole  reproduced  itself 
by  fission  with  each  cell  division  and  consequently  was  a  perma- 
nent organ  of  the  cell.  It  is,  however,  now  well  known  that  the 
large  central  space  containing  cell  sap  is  not  different  from  other 
vacuoles,  indeed  is  frequently  formed  by  the  flowing  together  of 
several  small  vacuoles  as  smaller  soap  bubbles  unite  in  the  froth 
to  form  a  larger  one  A  vacuolar  plasma  membrane  is  of  course 
bathed  by  water  since  it  holds  the  cell  sap  and  its  relation  to  a 
moist  surface  is  therefore  more  evident  than  in  the  case  of  the 
outer  plasma  membrane. 

The  third  plasma  membrane  encloses  the  nuclear  sap  with  the 
protoplasmic  nuclear  elements  chromatin,  linin  and  the  nucleolus. 
This  nuclear  membrane  was  discussed  in  connection  with  the 
nucleus  of  which  it  is  generally  considered  a  part,  but  as  there 
stated,  the  evidence  largely  indicates  that  it  is  cytoplasmic  in 
character,  representing  a  reaction  of  this  protoplasm  to  the  fluid 
nuclear  sap  formed  around  the  chromosomes  in  the  daughter 
nuclei  after  each  division  (Lawson  :c>3a).  The  nuclear  sap 


No.  449.]  STUDIES   ON  THE    PLANT  CELL. 

necessitates  the  development  of  a  vacuole  which  becomes 
bounded  by  the  nuclear  membrane.  The  nuclear  membrane 
in  some  cases  at  least  differs  from  a  vacuolar  membrane  in 
being  easily  distinguished  from  the  surrounding  cytoplasm  as 
a  definite  film. 

The  structure  of  all  the  plasma  membranes  is  much  the  same 
as  far  as  the  microscope  may  determine.  The  protoplasm  is 
dense,  colorless  and  filled  with  very  minute  granules  (micro- 
somata).  There  are  no  large  inclusions  such  as  plastids,  parti- 
cles of  food  material  (starch,  proteids,  oils,  fats,  etc.),  mineral 
matter  or  waste  products.  These  are  all  held  well  within  the 
cytoplasm  between  the  outer  plasma  membrane  and  the  vacuoles. 
There  is  good  reason  to  believe  that  the  substance  of  all  plasma 
membranes  is  much  the  same  since  they  perform  very  similar 
activities  both  in  relation  to  the  fluids  that  bathe  them  and  also 
because  their  substance  in  certain  cases  becomes  the  proto- 
plasmic basis  of  cellulose  walls.  These  resemblances  are  well 
established  for  the  outer  plasma  membrane  and  that  which  sur- 
rounds the  vacuoles.  Thus,  the  capillitium  of  Myxomycetes 
(Strasburger,  '84)  is  formed  from  the  plasma  membranes  around 
the  vacuoles  after  the  same  method  as  a  cell  wall  from  the  outer 
plasma  membrane.  And  again,  during  cleavage  by  constriction 
(see  section  II)  in  the  plasmodium  and  sporangium  of  the  molds 
(Harper,  '99  and  :  oo,  D.  Swingle,  :  03),  vacuoles  fuse  with  cleav- 
age furrows  from  the  outer  plasma  membrane  to  form  a  common 
membrane  which  surrounds  each  spore  mass  and  secretes  a  wall, 
thus  showing  identity  of  function  and  structure.  The  resem- 
blances are  less  conspicuous  for  the  kinoplasm  of  the  nuclear 
membrane,  only  appearing  indirectly  with  certain  events  of  cell 
division  (the  formation  of  the  cell  plate)  which  will  be  discussed 
in  the  next  section  of  the  paper.  The  evidence  indicates  that 
the  three  plasma  membranes  are  all  kinoplasmic  in  character,  a 
generalization  of  some  importance  since  it  offers  explanations  of 
many  peculiar  cell  activities  to  be  described  later. 

Since  all  plasma  membranes  have  these  common  characters  it 
may  well  be  questioned  whether  an  elaborate  terminology  is 
justified  for  structures  so  closely  related.  The  terms  ectoplast 
and  tonoplast  seem  undesirable  since  they  were  meant  to  indi- 


384  THE   AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

cate  peculiarities  of  structure  and  a  degree  of  permanence  as 
cell  organs  that  is  not  actually  present.  It  seems  hardly  neces- 
sary to  define  the  plasma  membranes  further  than  by  their  posi- 
tion in  the  cell  as  the  outer,  vacuolar  and  nuclear  membranes. 

All  of  the  cytoplasm  bounded  by  the  plasma  membranes  with 
the  exception  of  certain  conditions  to  be  described  later  (centre- 
spheres,  centrosomes,  asters,  filarplasm  and  blepharoplasts)  may 
be  called  trophoplasm  since  it  contains  structures  and  substances 
especially  concerned  with  nutritive  functions.  Trophoplasm 
presents  an  open  organization  in  sharp  contrast  to  the  dense 
kinoplasm.  This  peculiarity  is  due  in  part  to  numerous  small 
vacuoles  which  give  a  spongy  appearance  to  the  usual  foam  like 
structure  and  is  further  complicated  by  the  inclusion  of  material 
not  strictly  a  part  of  the  protoplasm  in  the  form  of  various  sized 
granules.  There  are  sometimes  present  fibrillae  that  impart  a 
somewhat  fibrous  texture.  We  cannot  discuss  here  the  theories 
of  the  structure  of  protoplasm,  which  has  not  been  so  extensively 
studied  in  plants  as  among  animals,  further  than  to  point  out 
that  it  varies  considerably  in  different  regions  of  the  cell  in 
relation  to  peculiarities  that  will  be  described  later.  There  is 
sometimes  presented  very  typically  the  foam  structure  of 
Butschli  but  the  introduction  of  small  vacuoles  generally  gives  a 
spongiose  appearance.  This  subject  is  critically  reviewed  by 
Fischer,  '99,  and  has  also  been  treated  in  several  papers  of 
Strasburger  especially  in  '97. 

Three  well  differentiated  organs  of  the  cell,  probably  tropho- 
plasmic  in  character,  require  special  mention,  viz.,  coenocentra, 
nematoplasts  and  physodes.  Coenocentra  are  very  interesting 
protoplasmic  centers  found  in  the  oogonia  of  certain  ccenocytic 
fungi  among  the  Saprolegniales  and  Peronosporales  during 
oogenesis.  They  appear  just  previous  to  the  differentiation  of 
the  eggs  as  small  bodies  sometimes  with  delicate  radiations  (see 
Fig.  3,  a  and  8,/),  and  are  found  one  in  each  egg  origin.  They 
are  apt  to  increase  in  size  as  the  eggs  mature  and  evidently 
become  the  centers  of  the  metabolic  activities  of  the  cells, 
drawing  the  sexual  nuclei  into  their  neighborhood  where  the 
latter  increase  in  size  (Fig.  3,  a  2).  The  ccenocentrum  dis- 
appears in  the  ripe  oospore  and  is  consequently  an  evanescent 


No'.  449.] 


STUDIES   ON   THE  PLANT  CELL. 


385 


structure.  It  is  probably  the  morphological  expression  of  a 
dynamic  center  in  the  egg.  Ccenocentra  have  been  known  for 
several  years  and  have  been  given  especial  attention  in  the 
recent  investigations  of  Stevens,  '99  and  'or,  and  the  author 
(Davis,  .-03).  They  will  be  further  considered  in  our  account  of 
Ccenogametes  (Section  III). 

Nematoplasts    are    exceedingly    small    rod    or    thread    like 


Fir,.  3. —  Cytoplasmic  structures,  a,  Coenocentra  of  Saprolegnia  ;  i,  oogonium,  each 
egg  origin  with  a  coenocentrum ;  2,  coenocentrum  and  nucleus  from  mature  egg. 
b,  Nematoplasts  from  hair  of  Momordica.  c,  Nucleus  from  apical  cell  of  Sphacela- 
ria,  aster  with  centrosome.  d,  Nucleus  from  oogonium  of  Fucus,  aster  with  centro- 
sphere.  e,  Nucleus  from  germinating  spore  of  Pellia,  centrospheres  with  short 
cytoplasmic  radiations  faster  like),  f,  Nucleus  from  procambium  cell  of  Vicia,  kino- 
I'plasmic  caps,  g,  Pollen  mother-cell  of  Lilium,  filarplasm  in  form  of  multipolar 
spindle.  A,  Development  of  sperm  of  Gymnogramme ;  i,  blepharoplast  at  side  of 
sperm  nucleus;  2,  blepharoplast  elongating  and  developing  cilia ;  3,  mature  sperm, 
blepharoplast  and  nucleus  in  parallel  bands,  cytoplasmic  vescicle  below.  After 
Zimmermann,  Hof,  and  Belajeff. 

structures  reported  by  Zimmermann  ('93,  p.  215)  in  the  cells  of 
hairs  of  Momordica  and  the  root  of  Vicia  (see  Fig.  36).  It  is 
probable  that  organs  described  by  Swingle,  '98,  and  Lagerheim, 
'99,  under  the  names  of  vibrioides  are  the  same  as  or  closely 


386  THE  AMERICAN  NATURALIST.  [VoL.  XXXVI I L 

related  to  physodes.  Swingle  found  them  in  some  of  the 
Saprolegniales  and  certain  Rhodophyceae  and  Lagerheim  in 
Ascoidea.  They  are  probably  not  uncommon.  Nematoplasts 
may  be  proteid  crystals  but  there  is  evidence  that  they  move, 
bending  slowly  back  and  forth,  which  suggests  a  higher  degree 
of  organization.  They  should  be  further  studied. 

Physodes  are  bladder  like  structures  described  by  Crato,  '92, 
in  certain  brown  Algae.  They  contain  a  highly  refractive  sub- 
stance which  gives  them  a  very  different  appearance  from 
vacuoles  whose  structure  they  resemble  in  many  respects. 
Very  little  is  known  about  the  contents  of  physodes  and  it  may 
well  be  questioned  whether  they  are  really  organs  of  the  cell 
and  not  vacuoles  set  apart  to  hold  some  fluids  or  substances 
other  than  cell  sap. 

There  are  left  for  us  a  group  of  kinoplasmic  structures  that 
are  especially  prominent  and  sometimes  only  present  during  the 
events  of  nuclear  division  and  at  the  times  when  cilia  are 
formed.  They  will  be  discussed  in  later  sections  of  these  papers 
(Sections  II,  III,  V  and  VI)  and  at  this  time  we  shall  give  but 
a  brief  statement  of  their  appearances.  They  are  centrospheres, 
centrosomes,  asters,  filarplasm  and  blepharoplasts. 

Centrospheres  are  rather  large  areas  of  kinoplasm  that  some- 
times lie  at  the  poles  of  nuclear  figures  and  to  which  are 
attached  the  fibrillae  that  form  the  spindle  and  also  those  that 
may  radiate  into  the  surrounding  cytoplasm.  If  the  centre- 
sphere  contains  a  distinct  central  body,  or  if  such  a  small 
structure  be  present  alone  at  the  poles  of  the  spindle  it  is  called 
a  centrosome.  Should  either  structure  be  accompanied  by 
definite  fibrillar  radiations  the  whole  is  termed  an  aster.  These 
latter  conditions  are  sometimes  very  complex  and  are  the  most 
interesting  types  of  structures.  Asters  with  centrosomes  are 
known  for  the  brown  algae  in  the  growing  points  of  Sphacelaria 
(Fig.  3c),  Stypocaulon  (Swingle,  '97)  and  the  spore  mother  cell 
of  Dictyota  (Mottier,  :oo).  They  are  also  beautifully  shown  in 
certain  diatoms  (Lauterborn,  principal  paper  '96,  Karsten,  :oo). 
Asters  with  centrospheres  and  occasionally  but  not  constantly 
containing  centrosome-like  bodies  are  found  in  the  oogonium 
and  germinating  eggs  of  Fucus,  see  Fig.  3,  d  (Strasburger,  '97*, 


No.  449.]  STUDIES   ON   THE  PLANT  CELL.  387 

Farmer  and  Williams,  '98).  Especially  well  differentiated  asters 
with  centrospheres  are  present  during  the  mitoses  in  the  ascus, 
functioning  at  the  end  in  the  peculiar  process  of  free  cell 
formation  (Harper,  '97).  Large  centrospheres  accompanied  by 
radiations  are  present  during  the  germination  of  the  spores  in 
certain  Hepaticae  (Farmer  and  Reeves,  '94,  Davis,  :oi,  Cham- 
berlain, :  03),  but  are  less  conspicuously  shown  in  some  and  are 
entirely  absent  in  other  phases  of  the  life  history.  Remarkably 
large  centrospheres  with  inconspicuous  radiations  are  known  in 
the  tetraspore  mother  cell  of  Corallina  (Davis,  '98).  Centro- 
spheres occur  in  the  basidium  (Wager,  '94,  Maire,  :  02).  Cen- 
trosomes  have  been  reported  during  the  mitoses  in  the 
sporangium  of  Hydrodictyon  (Timberlake,  :O2).  Centrosomes 
have  also  been  described  in  other  types  of  the  thallophytes  but 
we  are  justified  in  asking  for  further  work  on  these  bodies 
since  they  are  generally  without  raditions  and  may  not  have  at 
all  the  significance  indicated.  Neither  asters,  centrospheres  or 
centrosomes  seem  to  be  normally  present  in  groups  above  the 
bryophytes,  nuclear  division  taking  place  in  these  plants  by 
methods,  not  found  in  other  organisms,  which  will  be  described 
in  succeeding  sections. 

Vegetative  and  embryonic  tissues  of  plants  above  the  thallo- 
phytes present  very  different  conditions  from  those  described  in 
the  foregoing  paragraph.  The  centrosphere  is  replaced  by  a 
less  definite  structure  in  the  form  of  a  kinoplasmic  cap  which 
appears  at  the  ends  of  the  dividing  nucleus  and  determines  the 
poles  of  the  spindle  (see  Fig.  3,  /).  They  have  been  described 
in  the  cells  of  vegetative  points  of  several  pteridophytes  and 
spermatophytes  by  Rosen,  '93,  Hof,  '98,  and  Nemec,  '99  and  :  01, 
and  in  the  seta  and  late  divisions  in  the  germinating  spore  of 
the  liverwort  Pellia  (Davis,  :oi). 

The  most  highly  developed  conditions  of  spindle  formation 
are  found  in  the  spore  mother  cells  of  the  bryophytes,  pterido- 
phytes and  spermatophytes.  Here  the  nucleus  becomes 
surrounded  by  a  weft  of  fibrillae  which  form  a  kinoplasmic 
envelope  probably  derived  in  part  from  the  nuclear  membrane. 
The  fibrillae  are  at  first  quite  independent  of  one  another  or  of 
common  centers.  Most  of  the  fibrillas  enter  into  the  spindle 


388  THE  AMERICAN  NATURALIST.   [VOL.  XXXVIII. 

which  may  in  the  beginning  have  several  poles  (see  Fig.  3,^), 
but  these  generally  swing  at  last  into  a  common  axis  so  that 
the  spindle  finally  becomes  essentially  bipolar.  The  term 
filarplasm  is  applied  to  this  free  fibrillar  condition  of  kinoplasm 
without  organized  centers.  Filarplasm  is  peculiar  to  plant  cells 
and  its  remarkable  activities  in  connection  with  multipolar 
spindles  have  only  been  found  in  groups  above  the  thallophytes. 
Centrospheres,  centrosomes  and  asters  among  the  lower  plants 
resemble  in  general  the  same  structures  in  the  animal  cell.  But 
filarplasm  presents  a  higher  form  of  kinoplasmic  structure  with 
perhaps  the  most  complex  activities  known  in  the  process  of 
spindle  formation.  We  shall  consider  them  especially  in  Section 
III  when  treating  the  spore  mother  cell. 

The  blepharoplasts  are  in  some  respects  the  most  complex 
structures  derived  from  kinoplasm.  They  are  most  conspicuous 
in  the  sperm  cells  of  higher  plants  (spermatophytes  and 
pteridophytes)  but  they  are  undoubtedly  present  in  lower 
forms  and  probably  in  zoospores.  The  blepharoplast  develops 
cilia  as  delicate  fibrillae  from  its  surface.  The  origin  and  homol- 
ogies  of  the  blepharoplast  are  uncertain.  In  some  forms  they 
resemble  centrosomes  at  the  poles  of  the  last  nuclear  figures  in 
sperm  tissue.  But  in  other  cases  they  are  entirely  independent 
of  such  spindles,  a  character  which  cannot  be  brought  into 
harmony  with  the  activities  of  centrosomes.  They  finally  lie 
one  at  the  side  of  each  sperm  nucleus,  see  Fig.  3,  Ji,  and  with 
the  development  of  the  sperm  they  follow  the  spiral  twist,  when 
present,  as  a  parallel  band  (Fig.  3,  //,  2  and  3).  This  structure 
will  receive  detailed  treatment  in  our  account  of  the  sperm 
(Section  III). 

2.    Non  Protoplasmic  Contents. 

It  is  not  possible  to  distinguish  with  certainty  all  the  non- 
living material  of  a  cell  from  its  protoplasm.  We  have  at  one 
extreme  cells  from  which  the  protoplasm  has  almost  or  wholly 
disappeared  and  which  are  either  entirely  empty  or  set  apart 
solely  as  receptacles  for  various  substances,  sometimes  waste 
products  and  sometimes  food  materials.  In  contrast  with  this 


No.  449.]  STUDIES   ON   THE  PLANT  CELL.  389 

condition  are  the  cells  filled  with  cytoplasm  so  homogeneous  in 
structure  that  only  the  most  delicate  granules  (microsomata)  can 
be  distinguished  in  the  clear  substance. 

Waste  products  such  as  mineral  matter,  resins,  certain  oils, 
solutions  of  tannin  and  various  poisons,  such  as  the  alkaloides, 
may  be  easily  recognized.  Most  food  substances  such  as  starch, 
proteid  grains  (aleurone),  albumin  crystals,  oils,  fats,  etc.,  are 
readily  separated  from  the  protoplasm  in  which  they  lie.  But 
the  difficulties  are  much  greater  with  the  smaller  particles  of 
proteid  material,  which  are  frequently  such  minute  granules  as 
to  approach  the  microsomata  in  size.  These  may  give  to  the 
protoplasm  a  granular  consistency  that  breaks  up  the  foam  or 
spongiose  structure  characteristic  of  the  pure  condition.  These 
granules  are  undoubtedly  in  most  cases  substances  intimately 
concerned  with  the  metabolism  of  the  cell  and  are  members  of 
the  chains  of  constructive  and  destructive  processes  that  charac- 
terize life  phenomena. 

The  other  non  protoplasmic  structures  of  cells  are  vacuoles^ 
which  are  essentially  bubbles  of  fluid  lying  in  the  denser  proto- 
plasmic medium  and  surrounded  by  plasma  membranes.  The 
watery  fluid  of  vacuoles  contains  various  substances  in  solution, 
carbohydrates  such  as  the  sugars  glucoses  and  inulin,  mineral 
salts,  asparagin,  tannin,  alkaloids,  etc.,  and  occasionally  oil  and 
not  infrequently  crystals.  Vacuoles  may  be  formed  in  large 
numbers  in  protoplasm.  They  tend  to  run  together  as  do 
bubbles  in  a  froth  and  in  this  way  the  large  central  vacuole 
becomes  established  in  the  cell,  gathering  to  itself  many  smaller 
vacuoles  until  the  protoplasm  is  forced  to  lie  as  a  relatively  thin 
layer  next  the  cell  wall.  The  fluid  in  the  central  vacuole  (cell 
sap)  is  generally  thinner  and  more  watery  than  that  in  the 
smaller  vacuoles.  The  latter  are  apt  to  be  more  rich  in  albumen 
which  may  be  transformed  into  proteid  grains  as  is  especially 
well  illustrated  in  the  secretion  of  aleurone.  Cell  sap  may  be 
colored  by  pigments  in  solution  and  the  tints  of  flowers  are 
largely  due  to  this  cause  alone  or  to  the  effects  of  its  color  in 
combination  with  various  plastids  in  the  cell. 

It  is  possible  that  physodes,  described  among  the  cytoplasmic 
structures,  are  in  reality  vacuoles  filled  with  substances  other 
than  cell  sap,  which  are  not  as  yet  understood. 


390  THE   AMERICAN  NATURALIST.   [VoL.  XXXVIII. 

3.    The- Cell  Wall. 

Many  of  the  chief  peculiarities  of  plant  organization  and 
activities  are  due  to  the  presence  of  the  cell  wall,  its  influence 
on  structure  and  mode  of  life.  The  cell  wall  is  not  an  excretion 
from  the  cell  like  a  mineral  shell  but  is  formed  by  the  direct 
change  of  portions  of  the  protoplasm.  The  regions  concerned 
may  be  the  outer  plasma  membrane,  the  vacuolar  plasma  mem- 
brane or  the  substance  that  makes  up  the  spindle  fibers  which 
form  the  cell  plate.  These  structures  are  all  kinoplasmic  in 
character  and  have  to  do  with  the  formation  of  cell  walls  in 
various  ways  which  will  be  described  in  Section  II  under  the 
topic  "  The  Segmentation  of  the  protoplasm."  The  transforma- 
tion of  finely  granular  films  of  kinoplasm  into  cellulose  is  not 
well  understood  but  there  is  an  evident  solution  of  the  granules 
(microsomata)  and  the  change  of  the  resultant  substance  into 
the  cell  wall.  As  a  chemical  process  this  change  means  the 
replacement  of  molecules  of  an  albuminous  nature  by  those  of  a 
carbohydrate  substance.  The  most  complete  account  of  the 
cell  wall  is  that  of  Strasburger,  '98. 

Cell  walls  are  chiefly  composed  of  cellulose,  but  other  sub- 
stances are  always  present,  modifying  the  structure  in  various 
ways  to  give  widely  different  properties.  These  modifications 
are  generally  due  to  infiltrations  of  foreign  substances  but  some- 
times cell  walls  become  incrusted  with  mineral  deposits.  The 
group  of  cellulose  compounds  is  very  large  and  it  is  extremely 
difficult  to  identify  the  various  substances  in  structures  so  small 
as  the  cell  walls.  For  a  detailed  treatment  of  the  chemistry  of 
the  cellulose  group  the  reader  is  referred  to  Cross  and  Bevans, 
'95,  and  for  a  general  account  to  Pfeffer, :  oo,  p.  480-485 .  There 
are  microchemical  tests  for  cellulose  that  give  good  reactions 
for  most  tissues  but  which  cannot  be  relied  upon  for  some  walls 
(as  in  fungi  and  many  algae)  yet  it  is  well  understood  that  the 
cell  walls  of  these  organisms  are  from  the  biological  point  of 
view  essentially  the  same  as  for  other  plants.  The  cell  walls  of 
some  fungi  are  very  largely  composed  of  chitin. 

Several  substances  known  to  be  present  in  cell  walls  give 
them  marked  characteristics.  Their  association  with  the  cellu- 


No.  449-1  STUDIES   ON   THE   PLANT  CELL.  391 

lose  is  so  intimate  as  to  resist  very  severe  treatment  and  there- 
fore these  cell  walls  are  essentially  cellulose  groups  modified 
chiefly  in  their  physical  properties  by  the  presence  of  foreign 
substances.  The  most  conspicuous  modifications  of  this  charac- 
ter are  lignification,  suberization  and  cutinization.  Lignified 
walls  are  permeable  to  water  and  gases.  Several  substances 
have  been  separated  from  the  cellulose  of  lignified  walls,  among 
them  lignone,  coniferin,  vanillin,  etc.  Suberized  and  cutinized 
walls  are  largely  but  probably  never  wholly  impervious  to  water 
and  gases ;  the  one  is  infiltrated  with  suberin  and  the  other 
with  cutin,  substances  that  resemble  one  other  very  closely. 
Even  walls  that  appear  to  be  pure  cellulose  have  other  sub- 
stance united  with  them,  the  most  important  being  pectose  and 
callose.  Cell  walls  frequently  become  gelatinous  or  mucilaginous, 
when  the  outer  layers  swell  and  lose  their  form  or  they  may  be 
transformed  into  gums.  These  changes  are  well  illustrated  in 
the  coats  of  seeds  and  fruits  and  among  the  algae  and  fungi. 
The  cells  of  algae  frequently  secrete  gelatinous  envelopes  or 
sheaths  of  substances  so  closely  related  to  cellulose  that  were 
they  condensed  they  would  form  a  firm  cell  wall. 

The  cell  wall  may  grow  in  two  directions  by  methods  quite 
different  from  one  another.  There  is  first  surface  growth 
which  results  in  a  stretching  of  the  cellulose  membrane  (growth 
by  intussusception) .  And  second  there  may  be  growth  in  thick- 
ness by  the  formation  of  successive  layers  of  cellulose  inside  of 
one  another,  giving  the  wall  a  striated  structure  (growth  by 
apposition).  The  second  type  of  growth  is  chiefly  interesting 
since  it  makes  possible  many  peculiarities  of  structure,  because 
the  newly  formed  layers  may  not  be  deposited  uniformly  inside 
the  primary  wall.  In  some  cells  the  secondary  thickenings 
have  the  form  of  rings  or  spirals  or  a  reticulate  structure.  The 
reticulate  condition  passes  insensibly  into  the  pitted  cell  in  which 
the  secondary  layers  cover  the  greater  part  of  the  surface  leav- 
ing the  primary  wall  only  exposed  at  the  pits.  Further  dis- 
cussion of  these  cells  falls  more  within  the  range  of  histology 
than  the  purposes  of  this  paper. 

The  cell  wall  offers  a  very  interesting  field  of  research  among 
the  thallophytes  and  especially  in  the  lower  groups  where  we 


392  THE  AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

may  expect  to  find  these  envelopes  in  a  fairly  primitive  con- 
dition and  may  be  able  to  establish  the  steps  in  the  origin  and 
differentiation  of  this  very  important  accessory  structure  to  the 
plant  cell. 

( To  be  continued.") 


LITERATURE  CITED   FOR  SECTION   I  "THE  PLANT  CELL." 

CAVARA. 

'98.      Intorno  ad  alcune  strutture  nucleari.     Atti.  dell.   Inst.  hot.  Univ. 

di  Pavia,  II,  5,  1898. 
CHAMBERLAIN. 

'99.     Oogenesis  in  Pinus  laricio.     Bot.  Gaz.  27,  268,  1899. 
'03.     Mitosis  in  Pellia.     Bot.  Gaz.  36,  27,  1903. 
CRATO. 

'92.     Die    Physode,    ein    Organ    des  Zelllenleibes.       Ber.  d.    deut.   hot. 

Gesell.  10,  295. 
CROSS  AND  BEVAN. 

'96.     Cellulose,  an  outline  of  the  chemistry  of  the  structural  elements  of 

plants.      1895. 
DAVIS. 

'98.     Kerntheilung  in  der  Tetrasporenmutterzelle  bei  Corallina  officinalis 

L.  var.  mediterranea.     Ber.  d.  deut.  bot.  Gesell.  16,  266,  1898. 
'99.     The  spore  mother  cell  of  Anthoceros.     Bot.  Gaz.  28,  89,  1899. 
:01.     Nuclear  studies  on  Pellia.     Ann.  of  Bot.  15,  147,  1901. 
:03.      Oogenesis  in  Saprolegnia.     Bot.  Gaz.  35,  233  and  320,  1903. 
DEVRIES. 

'85.      Plasmolytische  Studien  iiber  die  Wand  der  Vacuolen  Jahrb.  f .  wiss. 

Bot.  16,  465,  1885. 
EBERDT. 

'91.     Beitrage    zur    Entstehungsgeschichte  der    Starke.     Jahrb.  f.  wiss. 

Bot.  22,  293,  1891. 
FARMER  AND  REEVES. 

'94.     On    the    occurrence    of    centrospheres  in  Pellia   epiphylla,   Nees. 

Ann.  of  Bot.  8,  219,  1894. 
FARMER  AND  WILLIAMS. 

'98.     Contributions  to  our  knowledge  of  the  Fucaceae ;    their  life  history 

and  cytology.     Phih  Trans.  Roy.  Soc.  190,  623,  1898. 
FISCHER. 

'99.     Fixirung,  Farbung  und  Bau  des  Protoplasmas.     Leipzig,  1899. 


No.  449-]  STUDIES   ON   THE   PLANT   CELL.  393 

HARPER. 

'97.     Kerntheilung  und  freie  Zellbildung  im  Ascus.     Jahrb.  f.  wiss.  Bot- 

30,  249,  1897. 

'99.     Cell  division  in  sporangia  and  asci.     Ann.  of  Bot.  13,  467,  1899. 
:00a.      Cell  and  nuclear  division  in  Fuligo  varians.     Bot.  Gaz.  30,  217,, 

1900. 
HOP. 

'98.     Histologische  Studien  an  Vegatationspunkten.     Bot.  Centb.  76,  65 1 


KARSTEN. 

:00.     Die  Auxosporenbildung  der  Gattungen    Cocconeis,  Surirella  und 

Cymatopleura.     Flora  87,  253,  1900. 
LAGERHEIM. 

'99.     Ueber  ein  neues  vorkommen  von  Vibrioiden  in  der  Pflanzenzelle. 

K.  Svenska.  Vet.  Akad.  Forhand.  No.  6,  1899. 
LAUTERBORN. 

'96.     Untersuchungen    iiber    Bau,    Kerntheilung    und     Bewegung    der 

Diatomeen.     Leipzig  1896. 
LAWSON. 

:  03a.     On  the  relationship  of  the  nuclear  membrane  to  the  protoplast. 

Bot.  Gaz.  35,  305,  1903. 
MAIRE. 

:02.     Recherches  cytologique  et    taxonomique    sur   les  Basidiomycetes. 

Bull.  d.  1.  Soc.  Mycol.d.  France.  18,  1902. 
MEYER. 

'83.     Ueber  Krystalloide  der  Trophoplasten  und  iiber  die  Chromoplasten 

der  Angiospermen.     Bot.  Zeit.  41,  489,  503,  525,  1883. 
'95.     Untersuchungen  iiber  die  Starkerkorner.     Jena  1895. 

MlTZKEWITSCH. 

'98.     Ueber  die  Kerntheilung  bei  Spirogyra.     Flora  85,  81,  1898. 
MOLL. 

'94.     Observations  sur  la  caryocinese  chez  les  Spirogyra.     Arch.  Neer. 

d.  Sci.  exactes  et  naturelle  28,  1894. 
MOTTIER. 

:OO.      Nuclear  and  cell  division  in  Dictyota  dichotoma.      Ann.  of  Bot.  14,. 

163,  1900. 
NEMEC. 
'99c.     Ueber  die  karyokinetische  Kernthielung  in  der  Wurzelspitze  von 

A  Ilium  cepa.     Jahrb.  f.  wiss.  Bot.  33,  313,  1899. 
:  01.     Ueber  centrosomahnliche  Gebilde  in  vegetativen  Zellen  der  Gefass- 

pflanzen.     Ber.  d.  deut.  bot.  Gesell.  19,  301,  1901. 
PALLA. 

'94.     Ueber  ein  neues  Organ  der  Conjugaten  Zelle.     Ber.  d.  deut..  bot. 

Gesell.  12,  153,  1894. 
PFEFFER. 

:  00.      The  physiology  of  plants.     Clarendon  Press  1900. 


394  THE  AMERICAN  NATURALIST.   [VOL.  XXXVIII. 

ROSEN. 

'95.     Beitrage  zur  Kenntniss  der  Pflanzenzellen  Cohn's  Beitr.  z.  Biol.  d. 
Pflan.  7,  225,  1895. 

S  ALTER. 

'98.     Zur  naheren  Kenntniss  der  Starkekorner.     Jahrb.  f.  wiss.  Bot.  32, 

117,  1898. 
SARGANTS. 

'97.     The  formation  of  sexual  nuclei  in  Lilium  Martagon,  II,  Sperma- 

togenesis.     Ann.  of  Bot.  11,  187,  1897. 
SCHIMPER. 

'81.     Untersuchungen  liber  das  Wachstum  der  Starkekorner.     Bot.  Zeit. 

39,   185,  1881. 
'85.     Untersuchungen    iiber    die    Chlorophyllkorper    und    die    in    ihnen 

homologen  Gebilde.     Jahrb.  f.  wiss.  bot.  16,  1885. 
SCHMITZ. 

'82.     Die  Chromatophoren  der  Algen.     Bonn.      1882. 
STEVENS. 

'99.     The  compound  oosphere  of  Albugo  Bliti.     Bot.  Gaz.  28,  149,  1899. 
'Olb.      Gametogenesis  and    fertilization  in   Albugo.     Bot.  Gaz.  32,  77, 

1901. 
STRASBURGER. 

'84.     Zur  Entwickelungsgeschichte  der  Sporangien  von    Trichia  fallax- 

Bot.  Zeit.  42,  305,  1884. 

'95.     Karyokinetische  Probleme.     Jahrb.  f.  wiss.  Bot.  28,  151,  1895. 
'97a.     Kerntheilung  und  Befruchtung  bei  Fucus.     Jahrb.  f.  wiss.  Bot.  30, 

351,  1897- 
'97b.     Ueber  Cytoplasmastructuren,  Kern  und  Zelltheilung.      Jahab.  f. 

wiss.  Bot.  30,  375,  1897. 

'98.     Die  pflanzlichen  Zellhaute.     Jahrb.  f.  wiss.  Bot.  31,  511,  1898. 
:  00.     Ueber     Reductionstheilung,     Spindelbildung,    Centrosomen      und 

Cilienbildner   im    Pflanzenreich.     Hist.  Beit.  6,   1900. 
SWINGLE,  W.  T. 

'97.     Zur  Kenntniss  der  Kern  und  Zelltheilung  bei  den  Sphacelariaceen. 

Jahrb.  f.  wiss.  Bot.  30,  297,  1897. 

'98.     Two  new  organs  of  the  plant  cell.     Bot.  Gaz.  25,  no,  1898. 
SWINGLE,  D. 

:  03.     Formation  of  spores  in  the  sporangia  of  Rhizopus  nigricans  and 

Phycomyces  nitens.     Bu.  Plant  Ind.  U.  S.  Dept.  Agri.  Bull.  37, 

1903. 

TlMBERLAKE. 

:01.     Starch-formation  in  Hydrodictyon  utriculatum.     Ann.  of  Bot.  15, 

619,  1901. 
:  02.     Development  and  structure  of  the  swarmspores  of  Hydrodictyon. 

Trans.  Wis.  Acad.  of  Sci.  Arts  and  Letters  13,  486,  1902. 


No.  449.]  STUDIES   ON   THE  PLANT  CELL. 


395 


VAX  WlSSELINGH. 

:00.     Ueber  Kerntheilung  bei  Spirogyra  II.     Flora  87,  355,  1900. 
:02.     Untersuchungen  iiber  Spirogyra  IV.     Bot.  Zeit.  60    HC^ioo2 
WAGER. 

'94.     On  the  presence  of  centrospheres  in  fungi.     Ann.  of  Bot.  8,  321, 
1894. 

ZlMMERMANN. 

'93  and  '94.     Sammel-Referate  aus  dem  Gesammtgebiete  der  Zellenlehre. 
Bei.  z.  bot.  Centb.  3  und  4,  1893-94. 

( To  be  continued.) 


VOL.  XXXVIII,  NO.  450  JUNE,  1904 

THE 

AMERICAN 
NATURALIST 


A   MONTHLY   JOURNAL 

DEVOTED  TO  THE  NATURAL  SCIENCES 
IN   THEIR    WIDEST   SENSE 


CONTENTS 

Page 

I.    Charles  Emerson  Beecher DR.  R.  T.  JACKSON  407 

n.    Variation  in  the  Bay  Flowers  of  the  Common  Cone  Flower  (Kudbeckia  hirta) 

F.  C.  LUCAS  427 

in-    Studies  on  the  Plant  Cell.- II DE.  BEADLEY  MOOE  DAVIS  431 

IV.    Notes  and  Literature :  Zoology,    Notes  on  Recent  Fish  Literature  —  Botany,  471 

Notes 474 

V-    Publications  Eeceived 479 


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STUDIES  ON  THE  PLANT  CELL.— II. 

BRADLEY  MOORE  DAVIS. 

THE  ACTIVITIES  OF  THE  PLANT  CELL. 
i.  Vegetative  Activities. 

EVERY  cell  passes  through  a  history  whose  events  repeat  in  a 
broad  way  activities  that  have  become  established  in  the  organ- 
ism by  the  experience  of  its  ancestors.  The  most  important  of 
these  events  is  nuclear  division,  which  is  accompanied  in  most 
plants  by  cell  division,  the  important  exceptions  being  certain 
groups  whose  protoplasm  is  multinucleate  throughout  all,  or 
almost  all,  vegetative  conditions  (e.  g.,  coenocytic  Algae  and 
Fungi,  plasmodia  and  multinucleate  cells  in  various  tissues). 

Protoplasm,  whose  nuclei  can  no  longer  divide,  becomes  inca- 
pable of  reproducing  itself  and  must  take  a  dependent  position 
in  the  organism,  where  the  length  of  its  life  will  be  determined 
by  the  good  fortune  of  its  environment  and  its  vitality.  Such 
protoplasm  becomes  strictly  vegetative  in  its  functions,  and  while 
these  activities  may  be  very  highly  specialized  and  of  the  utmost 
importance  to  the  organism  as  a  whole,  nevertheless  such  a  cell 
has  lost  certain  of  the  constructive,  and  in  consequence  repro- 
ductive, possibilities  characteristic  of  living  matter.  The  most 
evident  and  important  of  these  constructive  activities  have  to  do 
with  the  increase  of  nuclear  material  (chiefly  chromatin),  which 
leads  to  its  distribution  through  nuclear  division,  and  the  devel- 
opment of  a  complicated  mechanism  (the  spindle)  to  effect  this 
result. 

As  Weismann  first  pointed  out,  from  the  standpoint  of  cell 
studies,  there  is  a  stream  of  germ  plasm  flowing  with  every  spe- 
cies, protoplasm  relatively  fixed  in  its  characteristics  and  poten- 
tially immortal.  The  chief  peculiarities  of  germ  plasm  are  its 
reproductive  powers  and  the  generalized  structure  that  enables  it 

43' 


432  THE   AMERICAN  NATURALIST.   [VOL.  XXXVIII. 

to  turn  to  any  form  of  activity  possible  to  the  species.  Portions 
of  the  germ  plasm  are  constantly  being  detached  from  the  main 
stream  and  relegated  to  more  or  less  special  duties.  Such  pro- 
toplasm becomes  the  body  plasm,  or  soma,  of  the  individual. 
Specialized  body  plasm  generally  loses  very  shortly  the  reproduc- 
tive possibilities  of  germ  plasm,  ,and  in  consequence  must  finally 
die,  for  its  nicely  adjusted  dependence  upon  surrounding  cells 
cannot  last  forever.  Yet  it  has  been  one  of  the  surprises  of 
biological  science  that  specialized  tissues  may  keep  for  a  very 
long  time  the  reproductive  qualities  of  germ  plasm.  Investiga- 
tions on  regeneration  in  particular  have  brought  these  facts  con- 
spicuously to  the  front.  As  an  extreme  example  among  plants, 
it  is  known  that  even  the  epidermal  tissues  of  leaves  and  scales 
of  certain  ferns  (Palisa,  :  oo)  may  sometimes  retain  the  funda- 
mental qualities  of  germ  plasm  and  reproduce  the  plant. 

There  are  no  visible  characters  that  separate  body  plasm  from 
germ  plasm,  excepting,  of  course,  when  body  plasm  begins  to 
show  signs  of  degeneration.  Germ  plasm  may  only  be  distin- 
guished by  its  potentialities  of  growth  and  reproduction,  potenti- 
alities that  cannot  be  accurately  determined  because  the  stimulus 
to  development  is,  in  the  last  analysis,  an  external  one  and  the 
conditions  which  govern  it  may  be  so  intricate  as  to  escape  close 
scrutiny. 

Germ  plasm  is  found  in  its  most  generalized  condition  in  the 
cells  of  growing  points,  in  embryonic  and  meristematic  regions, 
and  in  the  reproductive  tissues.  These  tissues  are  well  recog- 
nized as  the  most  favorable  for  cell  studies  because  they  present 
most  clearly  the  details  of  protoplasmic  activities.  Almost  all 
that  we  know  of  cell  activities  have  come  from  investigations  of 
such  regions. 

One  of  the  first  signs  of  that  specialization  which  transforms 
germ  plasm  to  body  plasm  is  the  slowing  up  and  final  end 
of  nuclear  and  cell  division.  With  this  change  come  a  great 
variety  of  modifications  (peculiarities  of  cell  wall,  plastids,  cyto- 
plasmic  activities,  etc.)  which  may  be  readily  associated  with  the 
particular  work  of  that  tissue. 

The  vegetative  activities  of  germ  plasm  are  chiefly  those  of 
growth,  which  in  the  end  mean  reproduction,  the  embryonic  cells 


No.  450.]      .      STUDIES   ON   THE   PLANT  CE~LL.  433 

drawing  upon  food  that  has  been  prepared  for  them  and  is  either 
stored  in  special  structures  (as  seeds,  spores,  bulbs,  etc.),  or  manu- 
factured in  differentiated  organs  'or  tissues  (leaves,  chlorophyll 
bearing  tissue,  phlcem,  etc.).  The  vegetative  activities  of  body 
plasm  are  far  more  specific  than  those  of  germ  plasm.  Their 
tissues  have  particular  and  highly  developed  activities,  some  deal- 
ing chiefly  with  photosynthetic  processes,  some  (phlcem)  distrib- 
uting the  organized  food  over  the  plant  body,  some  storing  the 
food  in  large  quantities.  Besides  these  there  are  mechanical 
functions  performed  by  highly  differentiated  tissues,  even  though 
largely  composed  of  empty  cells,  as  the  vascular  tissue,  support- 
ing tissues,  and  the  external  protective  integuments. 

It  is  not  our  purpose  to  discuss  any  of  these  vegetative  activ- 
ities in  detail,  but  only  to  distinguish  as  sharply  as  possible  the 
characteristics  of  germ  plasm  with  its  generalized  activities  from 
the  specialized  body  plasm.  These  generalized  characters,  as 
before  stated,  are  constructive  activities  which  mean  growth  and 
lead  to  nuclear  and  cell  division.  It  is  probable  that  any  tissue 
which  presents  them  has  regenerative  powers  that  under  the 
proper  environment  might  be  expected  to  reproduce  parts  or  the 
entire  organism.  Germ  plasm  is  distributed  more  widely  through- 
out the  organism  than  is  generally  supposed,  and  many  highly 
specialized  tissues  still  retain  the  spark  of  regenerative  possi- 
bilities. The  significance  of  these  conditions  is  not  generally 
appreciated,  perhaps  because  the  environmental  conditions  of 
regeneration  are  little  understood  and  are  exceedingly  hard  to 
adjust  experimentally.  There  is  presented  here  a  very  attractive 
field  of  botanical  investigation,  a  union  of  cell  studies  with  the 
more  gross  anatomical  methods  of  experimental  morphology. 

2.    Cell  Division. 

Cell  division  takes  place  only  after  periods  of  growth  that 
have  led  to  a  multiplication  of  nuclei  and  in  the  tissues  of  plants 
above  the  thallophytes  is  very  generally  a  part  of  the  history  of 
each  mitosis.  This  is  because  of  the  structure  called  the  cell 
plate  which  is  essentially  an  organ  of  cell  division.  But  the 
thallophytes  present  other  methods  of  cell  division  which  bear 
no  especial  relation  to  nuclear  activities,  and  in  certain  groups  of 


434  THE  AMERICAN  NATURALIST.    [Vou  XXXV I II. 

the  thallophytes  nuclear  division  may  proceed  through  the  entire 
vegetative  life  of  the  organism  without  any  segmentation  of  the 
protoplasm  which  only  takes  place  during  the  reproductive  phase 
of  spore  formation.  But  fundamentally  protoplasmic  segmenta- 
tion depends  on  increase  in  the  amount  of  protoplasm  which 
demands  the  multiplication  of  nuclei  so  that  nuclear  division 
always  precedes  cell  division,  and  we  shall  consider  the  events  in 
that  order. 

(a)   Events  of  Nuclear  Division. 

i.    Direct  Division. 

The  nucleus  divides  after  one  or  two  methods,  either  directly 
by  constriction  or  fragmentation,  or  indirectly  (mitosis)  when 
there  is  present  a  fibrillar  apparatus  called  the  spindle.  Direct 
division  is  the  only  form  present  in  the  simplest  plants  and  phy- 
logenetically  must  have  preceded  the  elaborate  mechanism  de- 
manded for  indirect  division.  This  topic  will  be  given  especial 
attention  in  Section  VI '.  Direct  division  is  also  present  in  cer- 
tain specialized  cells  and  tissues  of  higher  plants.  These  are 
generally  old  cells  or  tissues  that  are  far  removed  from  the  gen- 
eralized structure  and  potentialities  of  germ  plasm.  Yet  some- 
times direct  and  indirect  division  occur  in  the  same  cell,  e.  g., 
Valonia  (Fairchild,  '94),  and  such  forms  might  be  made  the 
subject  of  very  interesting  investigations.  In  some  cases  the 
phenomenon  ,of  direct  nuclear  division  accompanies  pathological 
conditions  or  the  degeneration  of  cells  and  may  take  the  form  of 
extensive  fragmentation.  It  would  be  outside  of  our  purpose  to 
discuss  such  phenomena  which  is  obviously  abnormal,  and  the 
primitive  forms  of  nuclear  division  will  be  taken  up  later  (Sec- 
tion VI).  It  is  possible  that  direct  division  in  higher  plants  is  in 
a  sense  a  reversion  to  early  ancestral  conditions,  a  reversion  that 
only  comes  on  when  for  some  reason  the  normal  activities  of  the 
germ  cell  are  in  abeyance  or  have  ceased. 

2.    Indirect  Division  (Mitosis). 

Indirect  nuclear  division,  mitosis  or  karyokinesis,  is  character- 
ized by  a  mechanism  which  varies  greatly  among  plants  in  its 


No.  450.]  STUDIES   ON   THE   PLANT  CELL.  435 

method  of  development.  The  characteristic  appearance  of  this 
apparatus  is  a  spindle  like  figure  formed  of  fibrillae.  The  poles 
of  the  spindle  may  be  occupied  by  centrosomes  or  centrospheres 
or  they  may  be  entirely  free  from  such  organized  kinoplasmic 
bodies.  The  essential  structures  of  the  spindle  are  sets  of  con- 
tracting fibers  which  separate  the  chromosomes  into  two  groups 
drawing  them  to  the  poles  of  the  spindle  where  the  daughter 
nuclei  are  organized.  But  besides  these  fibers  there  are  gen- 
erally present  other  fibrillae  which  complicate  the  nuclear  figure. 
Some  of  these  extend  from  pole  to  pole  (spindle  fibers)  others 
lie  outside  of  the  spindle  and  end  freely  in  the  cytoplasm  or 
attach  themselves  to  chromosomes  (mantle  fibers),  and  if  centro- 
somes or  centrospheres  be  present  there  are  likely  to  be  fibers 
radiating  from  these  centers  to  form  asters. 

The  events  of  mitosis  are  generally  grouped  into  four  periods  : 
(a)  Prophase,  to  include  the  formation  of  the  spindle  and  prep- 
aration of  the  chromosome.s  ;  (b)  Metaphase,  the  separation  of 
the  daughter  chromosomes  ;  (c)  Anaphase,  the  gathering  of  the 
daughter  chromosomes  into  two  groups  which  pass  to  the  poles 
of  the  spindle  ;  (d)  Telophase,  the  organization  of  the  daughter 
nuclei.  It  is  almost  needless  to  say  that  these  periods  merge  so 
gradually  one  into  the  other  that  sharp  lines  cannot  be  drawn 
between  them.  The  activities  during  prophase  are  especially 
variable. 

Prophase.  —  There  are  two  types  of  spindles  in  plants,  ( i ) 
those  that  are  formed  within  the  nuclear  membrane  and  (2)  those 
whose  fibers  originate  largely  or  wholly  from  kinoplasm  outside 
of  the  nucleus.  Intranuclear  spindles  have  been  reported  in  a 
number  of  groups  of  the  thallophytes.  They  seem  to  be  the 
rule  in  the  mitoses  of  oogenesis  in  the  Peronosporales  (Wager, 
'96,  :oo,  Stevens,  '99,  :oi  and  :  02,  Davis,  :oo,  Miyake,  :oi, 
Trow,  :oi,  Rosenberg,  :O3).  They  are  present  in  Saprolegnia, 
Fig.  5a  (Davis,  103).  Fairchild  ('94)  reports  them  for  Valonia. 
Farmer  and  Williams  ('98,  p.  625)  state  that  the  spindle  of 
Ascophyllum  is  largely  intranuclear.  Harper  (:  oo)  has  not 
described  them  for  the  Myxomycetes,  but  very  little  is  known 
about  the  prophases  of  mitosis  in  that  group  and  their  presence 
is  quite  probable.  Timberlake  (:O2)  is  not  positive  whether  the 


436  THE   AMERICAN  NATURALIST.   [VOL.  XXXVIII. 

spindles  of  Hydrodictyon  are  intranuclear  or  not  ;  they  lie  in  a 
clear  space  which,  however,  may  be  a  vacuole  rather  than  the 
outline  of  a  nuclear  cavity.  It  seems  probable  in  such  a  type 
that  the  vacuole  is  really  the  nuclear  cavity  whose  plasma 
membrane  (nuclear  membrane)  becomes  less  clearly  defined. 
The  development  of  the  spindle  is  very  difficult  to  follow  among 
these  lower  forms  because  it  is  so  small.  Stevens  (103)  found 
an  exceptionally  favorable  type  in  Synchytrium  and  came  to 
the  conclusion  that  the  spindle  developed  from  the  threads  of 
the  spirem  (limn)  entirely  within  and  independent  of  the 
nuclear  membrane. 

Very  remarkable  intranuclear  spindles  have  been  described  in 
the  central  cell  of  the  pollen  tube  of  Cycas  (Ikeno,  '98  b)  and 
Zamia,  Fig.  5d  (Webber,  :oi).  Murrill  (:  oo)  found  them  in 
the  mitosis  following  the  fusion  of  gamete -nuclei  in  the  egg  of 
Tsuga,  Ferguson  (:oib)  at  the  same  period  for  pine,  and  Coker 
(:  03)  in  Taxodium.  They  are  also  reported  by  Strasburger  (:  oo) 
in  the  cells  of  young  anthers  and  nucelli  of  the  lily  and  in  grow- 
ing points  (Viscum)  and  possibly  may  be  found  quite  generally 
in  cells  weak  in  kinoplasmic  cytoplasm.  The  development  of 
the  spindles  in  the  above  forms  has  not  been  studied  in  detail, 
but  the  fibers  are  probably  derived  from  the  linin.  We  are 
given  a  clue  to  the  process  by  the  events  of  spindle  formation  in 
the  spore  mother  cell  of  Passiflora  (Williams,  '99).  In  this 
angiosperm  the  nuclear  cavity  becomes  filled  with  a  fibrillar 
network  developed  from  the  linin,  the  nuclear  wall  becomes 
transformed  into  a  mesh  connecting  the  intranuclear  fibers  with 
a  surrounding  cytoplasmic  reticulum.  The  fibers  in  the  central 
region  of  this  net  work  develop  the  spindle  which  is  consequently 
very  largely  of  intranuclear  origin. 

Among  the  thallophytes  the  poles  of  intranuclear  spindles  are 
frequently  occupied  by  deeply  staining  bodies  which  have  been 
called  centrosomes ;  but  these  structures  can  hardly  be  homol- 
ogous with  the  well-known  centrosomes  of  other  thallophytes, 
e.  g.,  Stypocaulon  (Swingle,  '97)  and  Dictyota  (Mottier,  :  oo). 
They  are  probably  merely  temporary  accumulations  of  material 
with  no  morphological  significance. 

Spindles  that  arise  from  fibers  external  to  the  nucleus  (extra 


No.  450.]  STUDIES   ON   THE  PLAWT~1?ELL.  437 


nuclear  spindles)  are  of  two  main  types  :  (i)  those  associated 
with  centrosomes,  centrospheres  or  kinoplasmic  caps,  and  (2) 
those  composed  of  independent  fibrillae  developed  as  a  mesh 
around  the  nucleus.  The  latter  condition  is  especially  character- 
istic of  the  spore  mother  cell  and  is  perhaps  the  highest  type  of 
spindle  formation  known  for  either  animals  or  plants.  It  is  very 
interesting  to  trace  the  relations  of  this  highest  condition  to  the 
lower  types  through  certain  lines  of  evolution  to  be  discussed  in 
Section  VI. 

Spindles  with  centrosomes  are  known  in  Sphacelaria,  Stypo- 
caulon  (Swingle,  '97),  Dictyota,  Fig.  4  a  (Mottier,  :  oo),  the  zoo- 
sporangium  of  Hydrodictyon  (Timberlake,  :  02),  in  certain 
diatoms  (Lauterborn,  principal  paper  '96,  Karsten,  :  oo)  and  in 
the  basidium  (Wager,  '94  and  Maire,  :O2).  The  best  accounts 
of  the  behavior  of  the  centrosomes  are  given  by  Swingle  and 
Mottier.  Indeed  there  is  much  doubt  about  the  history  and 
significance  of  the  bodies  in  the  other  forms,  although  the  con- 
stancy of  their  presence  at  the  poles  of  the  spindles  indicates 
that  they  are  really  centrosomes.  The  conditions  in  the  diatoms 
are  especially  complicated  ;  an  account  of  Lauterborn's  work  has 
been  published  in  English  by  Rowley,  :o3.  In  Stypocaulon, 
Sphacelaria  (Fig.  3  c,  Section  I)  and  Dictyota  (Fig.  4  a)  the  cells 
studied  have  permanent  asters  which  lie  at  the  side  of  the 
nucleus  and  which  divide  just  previous  to  the  mitosis  and  sep- 
arate so  that  they  come  to  lie  on  opposite  sides  of  the  nucleus. 
Fibers  develop  from  the  centrosomes  on  the  sides  nearest  the 
nucleus  and  elongating  push  against  the  nuclear  membrane  and 
finally  enter  the  nuclear  cavity  to  form  the  spindle. 

Spindles  with  centrospheres  are  well  known  in  Fucus  (Farmer 
and  Williams,  '96,  '98,  Strasburger,  '9/a),  Corallina,  Fig.  5  c, 
(Davis,  '98),  in  the  ascus,  Fig.  5  b  (Harper,  '97  and  '99),  and  in 
the  germinating  spore  of  Pellia,  Fig.  4  c  (Farmer  and  Reeves, 
'94,  Davis,  :oi,  Chamberlain,  :O3).  Centrospheres  have  been 
reported  in  other  forms  but  the  types  mentioned  above  have 
received  the  most  careful  study.  It  is  probable  that  the  centro- 
sphere  is  but  a  larger,  more  generalized  kinoplasmic  center  than 
the  centrosome,  a  protoplasmic  region  whose  dynamic  activities 
do  not  focus  so  sharply  as  in  the  latter  structure.  There  are 


438  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

bodies,  as  in  the  basidium,  which  stand  intermediate  in  size 
between  centrosomes  and  centrospheres  and  are  probably  only 
called  the  former  because  they  are  very  distinct  in  outline. 

Centrospheres  in  Fucus  (Fig.  3  d,  Section  I),  Corallina  (Fig. 
4  b}  and  Pellia  (Fig.  3  e,  Section  I,  Fig.  4  c)  are  formed  de  novo 
for  each  mitosis  by  an  accumulation  of  kinoplasm  at  the  poles  of 
the  elongating  nucleus.  The  centrospheres  in  the  ascus  divide 
before  each  of  the  three  successive  mitoses  and  finally  remain, 
one  for  each  nucleus,  to  instigate  the  peculiar  process  of  free 
cell  formation  characteristic  of  the  ascus.  Centrospheres  are 
frequently  the  centers  of  asters  which,  however,  are  usually  not 
as  sharply  denned  as  those  with  centrosomes,  possibly  because 
the  fibers  are  not  grouped  with  the  same  degree  of  symmetry  as 
is  shown  around  controsomes. 

Spindle  fibers  from  centrospheres  develop  in  precisely  the 
same  manner  as  from  centrosomes,  i.  e.  by  the  growth  of  the 
fibrillae  into  the  nuclear  cavity  through  the  dissolving  nuclear 
membrane.  The  activity  is  well  shown  in  the  oogonium  of 
Fucus,  and  Farmer  ('98,  p.  638)  believes  "that  the  intranuclear 
part  of  the  spindle  is  differentiated  out  of  nuclear  material  that 
is  unused  for  chromosome  formation."  The  entrance  of  spindle 
fibers  from  centrospheres  at  the  ends  of  a  nucleus  has  been 
observed  by  myself  in  Corallina,  Fig.  4  b  (Davis,  '98).  The 
germinating  spores  of  Pellia,  Fig.  4  c  (Davis,  :oi,  Chamberlain, 
:  03)  furnish  especially  good  illustrations  of  the  entrance  of  spin- 
dle fibers  into  the  nuclear  cavity  and  the  development  of  the 
spindle  in  this  form  is  coincident  with  the  dissolution  of  the 
nucleus  which,  according  to  Strasburger's  theory  ('95),  indicates 
that  the  latter  structure  contributes  material  for  the  growth  of 
spindle  fibers. 

In  connection  with  the  centrosphere  mention  should  be  made 
of  the  blepharoplasts  of  the  cycads  and  Ginko  which  are  remark- 
able bodies  with  radiating  fibers.  They  have  been  considered 
by  some  as  asters  with  centrosomes,  but  it  is  known  that  they 
take  no  part  in  spindle  formation  or  other  mitotic  phenomena  in 
these  forms,  and  consequently  need  not  be  considered  at  this 
time.  They  will  be  treated  in  some  detail  in  the  account  of  the 
sperm  (Section  III). 


No.  450.] 


STUDIES   ON   THE    PLANT  CELL. 


439 


Kinoplasmic  caps  which  form  spindles  are  probably  an  evolu- 
tion from  the  type  of  centrosphere  that  is  developed  de  novo 
with  each  mitosis  as  in  Pellia.  Such  centrospheres  by  -becoming 
less  definite  in  form  and  lacking  radiating  fibers  would  be  called 
kinoplasmic  caps.  Indeed  the  centrosphere  so  evident  in  the 
early  cell  divisions  of  the  germinating  spore  of  Pellia  becomes  a 
kinoplasmic  cap  in  the  later  mitoses  of  the  older  gametophyte 
(Davis,  :oi). 

Spindles  developed  from  kinoplasmic  caps  are  characteristic  of 


FIG.  4. —  Prophases  of  Mitosis,  a.  Dictyota  ;  late  prophase  in  spore  mother  cell,  fibers  from 
the  two  asters  with  centrosomes  have  entered  nuclear  cavity  to  organize  the  spindle,  chro- 
mosomes gathering  to  form  the  nuclear  plate,  b,  Corallina,  early  prophase  in  tetra  spore 
mother  cell;  two  centrospheres,  the  fibers  for.n  one  having  entered  the  nuclear  cavity, 
chromosomes  shown,  c ,  Pellia,  nucleus  in  germinating  spore  ;  spindle  fibers  from  ill 
defined  centrospheres  entering  nuclear  cavity,  chromosomes  and  a  nucleolus  present,  d, 
Gladiolus,  first  mitosis  in  pollen  mother  cell ;  a  multipolar  spindle,  nuclear  wall  breaking 
down  at  one  side  and  fibrillse  entering  the  nuclear  cavity,  chromosomes  and  a  nucleolus 
present.  After  Mottier  and  Lawson. 

the  mitoses  in  vegetative  tissues,  meristematic  and  other  embry- 
onic regions.  They  have  been  especially  studied  in  higher  plants 
by  several  investigators  and  for  a  large  number  of  forms,  those 
most  completely  described  being  Psilotum  (Rosen,  '95),  Equise- 
tum,  Allium  and  Solanum  (Nemec,  'Q8a  and  '98b,  *99b  and  '99c), 
Pteris,  Ephedra  and  Vicia,  (Fig.  3  /,  Section  I)  (Hof,  '98)  and 
Allium  (McComb,  :oo).  The  polar  caps  first  appear  as  accumu- 
lations of  kinoplasm  on  opposite  sides  of  the  nucleus  which 
generally  elongates.  The  protoplasm  is  granular  and  although 


440  THE   AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

central  bodies  have  been  reported  most  investigators  are  agreed 
that  they  are  only  granules  without  regularity  or  special  signifi- 
cance. They  are  no  longer  believed  to  be  centrosomes.  Fibrillae 
are  developed  from  the  kinoplasmic  caps  and  grow  out  against 
the  nuclear  membrane  and  finally  enter  the  nuclear  cavity  to  form 
the  spindle.  A  large  part  of  the  substance  of  the  kinoplasmic 
cap  is  transformed  into  these  spindle  fibers. 

Papers  by  Schaffner  ('98)  on  Allium  and  Fulmer  ('98)  on  the 
seedling  of  the  pine  are  the  last  attempts  to  bring  the  centro- 
some  into  the  history  of  spindle  formation  in  vegetative  tissues 
of  higher  plants.  But  their  results  cannot  stand  against  the 
accumulation  of  studies  which  indicate  that  centrosomes  are  not 
present  in  the  cells  of  any  plant  above  the  thallophytes  with  the 
possible  exception  of  the  mysterious  blepharoplast  and  certain 
structures  appearing  in  some  phases  in  the  life  history  of 
Hepaticae.  Centrospheres  are  unquestionably  present  in  the 
Hepaticoe  and  centrosomes  have  also  been  reported.  The 
centrospheres  are,  however,  so  generalized  as  to  approach  the 
kinoplasmic  caps  in  structure  and  development  and  it  seems 
quite  possible  that  they  are  the  forerunners  of  this  manifesta- 
tion of  kinoplasm.  The  so-called  centrosomes  of  the  liverworts 
do  not  exhibit  the  specialized  structure  or  behavior  of  cen- 
trosomes among  the  thallophytes  and  it  is  probable  that  they 
are  only  smaller  and  somewhat  more  clearly  defined  centro- 
spheres. These  structures  in  the  Hepaticae  seem  to  hold  an 
intermediate  relation  between  the  definite  kinoplasmic  bodies 
(asters,  centrosomes  and  centrospheres)  of  the  thallophytes  and 
the  remarkable  kinoplasmic  activities  in  higher  plants  which 
reach  their  highest  expression  in  the  processes  of  spindle  forma- 
tion in  the  spore  mother  .cell.  These  topics  will  be  treated  in 
Section  VI. 

Structures  resembling  kinoplasmic  caps  have  been  reported  in 
several  other  tissues  than  those  noted  above.  Thus  Murrill 
(:oo)  finds  in  the  formation  of  the  ventral  canal  cell  of  Tsuga  a 
dense  fibrous  accumulation  beneath  the  nucleus  which  develops 
one  pole  of  the  spindle  in  essentially  the  same  manner  as  other 
polar  caps.  The  other  pole  of  the  spindle  in  this  case  appears 
to  be  formed  differently  for  the  fibers  seem  to  be  intranuclear. 


No.  450.]  STUDIES   ON  THE  PLANT  CELL.  441 

It  would  be  interesting  if  two  types  of  spindle  formation  were 
present  at  opposite  pole$  of  the  same  nucleus  and  further  inves- 
tigation of  this  subject  is  much  to  be  desired.  The  mitoses  in 
the  central  cell  of  Pinus  (Ferguson,  :oib,  Chamberlain,  '99, 
and  Blackman,  '98)  and  Picea  (Miyake  :  O3a)  show  spindle  for- 
mation from  accumulations  of  fibrillae  outside  of  the  nucleus  but 
without  conspicuous  polar  caps.  Still  more  striking  than  the 
irregular  spindle  of  Murrill  in  Tsuga,  described  above,  is  Miss 
Ferguson's  (:oia)  account  of  the  mitosis  in  the  generative  cell 
of  the  pollen  grain  of  Pinus.  The  spindle  here  begins  to  develop 
as  a  cap-like  accumulation  of  kinoplasm  below  the  nucleus.  The 
fibers  enter  the  nuclear  cavity  and  in  cooperation  with  a  nuclear 
reticulum  form  a  system  of  fibers  that  extend  through  the 
nuclear  cavity  to  the  inner  side  of  the  nuclear  membrane 
beyond.  This  portion  of  the  nuclear  membrane  persists  until 
after  metaphase  so  that  one  pole  of  the  spindle  is  found  wholly 
within  the  nucleus  while  the  other  is  external  and  of  unques- 
tioned cytoplasmic  origin.  Coker,  :  03,  regards  the  spindle  which 
differentiates  the  nucleus  of  the  ventral  canal  cell  in  Taxoclium 
as  almost  wholly  of  nuclear  origin  and  the  chromosomes  as 
derived  largely  from  the  nucleolus.  There  are  evidently  some 
interesting  complications  in  this  form  which  deserve  further 
study. 

It  should  be  noted  that  whenever  spindles  are  formed  in  con- 
nection with  centrosomes,  centrospheres  or  kinoplasmic  caps  that 
the  fibers  have  a  definite  region  of  attachment  from  which  they 
extend  into  the  nuclear  cavity.  Such  regions  constitute  a  sort 
of  anchorage  for  the  spindle  fibers.  In  this  respect  the  physi- 
ological side  of  the  process  of  spindle  formation  in  these  forms 
is  quite  similar  to  that  of  the  animal  kingdom  and  in  sharp 
contrast  to  other  methods  that  are  found  in  higher  plants,  which 
will  now  be  considered. 

When  spindles  are  formed  after  the  second  method,  i.  <?., 
by  independent  fibrillae  making  up  a  network  around  the  nucleus, 
there  is  an  abrupt  change  in  the  method  of  development. 
The  kinoplasm  becomes  distributed  around  the  nucleus  as  an 
investing  layer  and  shows  no  inclination  to  gather  into  centers 
such  as  kinoplasmic  caps  or  centrospheres.  There  is  developed 


442  THE  A  ME  RICA  N  NA  TURA  LIST.   [VOL.  XXX  V 1 1 1 . 

from  this  granular  kinoplasm  a  meshwork  of  fibrillae  that  extends 
into  the  cytoplasm  more  or  less  radially.  When  the  nuclear 
membrane  becomes  disorganized  the  fibers  enter  the  nuclear 
cavity  and  organize  the  spindle  (see  Fig.  4  d}.  In  some  forms, 
e.g.,  Passiflora  (Williams,  :  oo),  many  or  most  of  the  fibers  are 
developed  in  the  interior  of  the  nucleus  from  the  linin  and  become 
connected  with  the  extra  nuclear  reticulum  by  the  dissolution  of 
the  nuclear  membrane. 

The  free  ends  of  the  fibrillae  that  lie  in  the  cytoplasm  become 
gathered  into  several  poles  which  are  distributed  variously  around 
the  nucleus.  This  condition  constitutes  the  so-called  multipolar 
spindle  (Fig.  $g,  Fig.  4<^),  which  in  its  highest  type  of  develop- 
ment illustrates  the  most  complex  method  of  spindle  formation 
known  for  animals  or  plants.  During  the  later  periods  of 
prophase  the  several  poles  of  the  multipolar  spindle  converge 
and  fuse  with  one  another  into  two  poles  with  a  common  axis, 
thus  forming  the  mature  bipolar  spindle  of  metaphase  (Fig.  5/). 
The  spindle  is  in  a  broad  sense  bipolar,  but  one  may  readily  see 
that  each  pole  is  made  up  of  several  groups  of  fibrillae  which 
generally  remain  quite  independent  of  one  another  (Fig.  $fi}. 

The  relation  of  a  multipolar  stage  to  the  bipolar  spindle  of 
metaphase  was  first  made  clear  by  Belajeff  (*94b)  for  Larix,  and 
later  was  established  more  widely  by  the  investigations  of  Oster- 
hout  ('97)  on  Equisetum,  Mottier  ('97)  for  the  lily,  and  Juel  ('97) 
for  Hemerocallis.  This  type  of  spindle  formation  is  now  well 
known  in  the  spore  mother  cells  of  numerous  spermatophytes 
and  several  pteridophytes.  The  same  conditions  in  simpler 
form  are  found  in  the  spore  mother  cells  of  the  Hepaticae, 
e.g.,  Anthoceros  (Davis,  '99),  Pellia,  Fig.  5  e  (Davis,  :oi),  and 
Pallavicinia  (Moore,  '.03).  There  are  a  number  of  very  interest- 
ing peculiarities  in  this  type  of  spindle  which  presents  a  wide 
range  of  variation  in  the  details  of  its  fibrillar  organization  and 
development.  These  will  receive  special  treatment  in  the  account 
of  the  spore  mother  cell  (Section  III). 

The  only  types  of  thallophytes  known,  in  which  the  spindle  is 
partly  or  wholly  of  cytoplasmic  origin  without  centrosomes,  cen- 
trospheres,  or  kinoplasmic  caps,  are  Chara  (Debski,  '97)  and 
Spirogyra  (Van  Wisselingh,  :O2).  The  developmental  history  is 


No.  450.]  STUDIES   ON  THE  PLANT  CELL.  443 

very  difficult  to  follow  in  these  forms  and  is  not  fully  known,  but 
multipolar  conditions  are  reported  which  later  change  into  bipolar 
spindles. 

While  the  spindle  is  being  organized  by  kinoplasmic  activities 
outside  of  the  nucleus,  some  events  occur  within  which  form  a 
very  important  part  of  the  prophases  of  mitosis.  The  linin 
material,  which  in  the  resting  nucleus  generally  has  the  form  of 
a  net,  becomes  organized  into  a  much  looped  ribbon,  called  the 
spirem  thread.  The  chromatin  material  gathers  along  the  spirem 
thread  as  deeply  staining  globular  bodies.  These  split  into  halves 
in  the  direction  parallel  with  the  axis  of  the  spirem  thread,  and 
the  two  sets  of  chromatic  bodies  lie  in  two  rows  along  the  edge 
of  the  ribbon,  which  shortens  as  it  grows  older.  Finally  the 
spirem  thread  divides  transversely  into  a  definite  number  of  seg- 
ments, and  these  are  the  chromosomes.  The  chromosomes  are 
generally  fully  formed  at  the  time  when  the  spindle  fibers  enter 
the  nuclear  cavity,  and  they  are  readily  moved  as  the  fibrillae 
develop  the  spindle.  Some  of  the  fibers  become  attached  to  the 
chromosomes,  carrying  them  to  the  equatorial  region  of  the 
spindle  to  form  the  structure  called  the  nuclear  plate,  which 
always  indicates  the  approach  of  metaphase. 

As  the  spirem  thread  matures  the  amount  of  chromatin  is 
greatly  increased,  so  that  the  separate  globules  run  together  and 
cannot  be  distinguished  in  the  chromosome  which  is  homogeneous 
in  structure.  Chromatin  has  its  greatest  staining  power  at  this 
period.  Whether  linin  is  closely  related  to  chromatin  in  compo- 
sition and  is  actually  changed  into  that  substance,  or  whether  it 
dissolves  and  contributes  its  material  to  the  growth  of  the  spin- 
dle, is  a  problem  of  some  importance  as  yet  unsolved.  It  is 
possible  that  the  nucleolus  may  furnish  material  for  the  chromo- 
somes, and  some  nucleolar  like  bodies  are  known  to  be  chromatic 
in  character,  but  it  does  not  seem  to  be  established  that  any  of 
these  are  genetically  related  to  an  unquestioned  nucleolus  in  any 
plant  form. 

Important  changes  come  over  the  nucleolus  coincident  with  the 
development  of  the  chromosomes.  The  structure  frequently 
gives  signs  of  internal  modifications  early  in  prophase  and  before 
the  development  of  the  spindle.  It  may  gradually  fade  away  or 


444  THE  AMERICAN  NATURALIST.   [VOL.  XXXVIII. 

decrease  in  size,  or,  if  large,  it  may  fragment.  Strasburger,  in 
1895,  advanced  the  view  that  the  spindle  actually  drew  upon  the 
substance  of  the  nucleolus  for  the  material  and  energy  necessary 
to  its  development.  The  evidence  in  support  of  this  suggestive 
theory  lies  chiefly  in  the  development  of  the  spindle  coincident 
with  the  dissolution  of  the  nucleolus.  There  is  also  some  evi- 
dence that  the  nucleolus  contributes  material  to  the  developing 
chromosomes.  Small  globules,  which  stain  as  the  substance  of 
the  nucleolus,  may  sometimes  be  found  adhering  to  the  chromo- 
somes as  though  becoming  incorporated  in  them.  These  sub- 
jects are  naturally  very  difficult  of  investigation  because  stain 
reactions  cannot  be  depended  upon  with  certainty  and  are  not, 
of  course,  chemical  tests.  Then  the  behavior  of  the  nucleolus 
during  mitosis  is  exceedingly  variable,  since  it  sometimes  disap- 
pears quickly  and  sometimes  remains  intact,  and  it  becomes  a 
very  difficult  matter  to  determine  its  importance.  The  nucleolus 
is  probably  not  absolutely  necessary  at  any  stage  in  mitosis,  for 
both  spindle  fibers  and  chromosomes  develop  apart  from  this 
structure ;  but  it  does  seem  to  be  established  that  the  substance 
of  the  nucleolus  is  generally  drawn  upon  by  the  cell,  especially 
during  prophase,  when  numerous  spindle  fibers  are  organized  and 
the  amount  of  chromatin  is  being  largely  increased.  Experi- 
ments of  Hottes,  which  unfortunately  have  never  been  published, 
have  an  important  bearing  on  these  problems. 

If  the  nucleoli  are  not  entirely  dissolved  they  are  frequently 
thrown  out  of  the  spindle  into  the  cytoplasm,  where  they  may 
lie  for  long  periods  as  deeply  staining  globules  which  are  some- 
times called  extra  nuclear  nucleoli.  It  is  probable  that  very  many 
of  the  bodies  that  pass  under  this  cumbersome  title  have  no 
relation  whatever  to  the  nucleolus.  The  cytoplasm  frequently 
contains  globules  that  may  be  coagulated  or  precipitated  food 
products,  and  all  of  these  stain  similarly  to  nucleoli. 

Metaphase.  —  The  period  of  mitosis  termed  metaphase  is,  to 
speak  precisely,  the  time  when  the  two  halves  of  the  split  chromo- 
some separate  from  one  another.  However,  this  is  a  period  of 
such  short  duration  that  for  practical  purposes  nuclei  are  consid- 
ered in  metaphase  when  their  chromosomes  are  lined  up  at  the 
nuclear  plate.  The  metaphase  of  mitosis  is  generally  the  most 


No.  450.] 


STUDIES   ON   THE  PLANT  CELL. 


445 


conspicuous  of  the  nuclear  activities  not  only  on  account  of  the 
position  of  the  chromosomes  (see  Fig.  5),  but  because  all  kino- 
plasmic  structures  (the  nbrillae  and  centrosomes  or  centrospheres, 
if  present)  are  shown  to  their  best  advantage. 

The  best  evidence  indicates  that  the  chromosomes  of  plants 


FIG.  5. —  Metaphases  of  Mitosis,  a,  Saprolegnia ;  intranuclear  spindle  in  oogonium,  nucle- 
olus  outside  of  spindle.  6,  Erysiphe  ;  mitosis  in  ascus,  asters  with  rather  small  centro- 
spheres. c,  Corallina  ;  first  mitosis  in  tetraspore  mother-cell,  very  large  and  well 
differentiated  centrospheres.  d,  Zamia ;  blunt  poled  intranuclear  spindle  in  central  cell 
of  pollen  grain  ;  blepharoplasts,  their  outer  membrane  about  to  break  up.  e,  Pellia ;  first 
mitosis  in  spore  mother-cell;  broad  spindle  with  rounded  poles,  the  very  numerous  spin- 
dle fibers  ending  in  granular  kinoplasm.  /,  Agave;  first  and  second  mitoses  in  pollen 
mother-cells  ;  (i),  multipoiar  spindle  just  previous  to  metaphase ;  the  several  independent 
cones  of  fibrills  gather  more  closely  together  to  complete  the  spindle.  (2)  metaphase  of 
second  mitoses  ;  completed  spindles  showing  however  the  several  independent  cones  of 
fibrills.  (After  Harper,  Webber  and  Osterhout.) 

only  divide  longitudinally.  This  matter  has  considerable  theo- 
retical interest,  which  will  be  considered  in  Section  V,  and  also 
in  connection  with  the  spore  mother  cell  (Section  III).  The 
daughter  chromosomes  are  drawn  apart  by  the  contraction  of  the 
fibrillae  to  which  they  are  attached. 

Chromosomes  may  take  on  various  forms  during  metaphase, 


446 


THE  AMERICAN  NATURALIST.   [VOL.  XXXVIII. 


especially  while  they  are  being  separated.  Thus,  if  the  chromo- 
somes are  dragged  apart  from  the  ends,  their  form  is  generally 
rod  shaped ;  but  if  the  attachment  of  the  fibrillae  is  near  the 
middle  of  the  chromosome,  the  structures  are  pulled  apart  as 
loops  or  V's,  and  the  pair  of  chromosomes  just  previous  to  their 
separation  may  be  ring  shaped.  A  further  complication  is  intro- 
duced in  the  spore  mother  cell  by  certain  premature  divisions  by 
which  each  daughter  chromosome  becomes  a  pair  of  granddaugh- 
ter chromosomes  instead  of  remaining  a  single  structure.  The 
peculiarities  of  the  heterotypic  and  homotypic  mitoses  are  due 


FIG.  6. —  Anaphase  of  Mitosis,  spore  mother-cell  of  Lilium  martagon.  a,  immediately 
after  metaphase  of  first  mitosis;  each  daughter  chromosome  consists  of  two  grand 
daughter  segments,  adhering  at  the  ends,  making  the  familiar  V-shaped  figures  charac- 
teristic of  the  first  mitosis  (heterotypic)  in  the  spore  mother-cell  of  higher  plants,  b,  late 
anaphase  of  the  first  mitosis;  the  V  shaped  chromosomes,  each  composed  of  two  grand 
daughter  segments  adhering  at  the  ends,  are  very  close  to  the  poles  of  the  spindle  ;  the 
central  fibers  of  the  spindle  are  conspicuous  at  this  stage,  c,  second  mitosis  ;  the  grand 
daughter  chromosomes,  that  composed  the  Vs  of  the  first  mitosis,  have  separated  at  the 
nuclear  plate  of  the  second  mitosis  and  are  being  drawn  by  their  ends  to  the  poles  of  the 
spindle  where  they  will  organize  the  nuclei  of  the  pollen  grain;  this  mitosis  is  called 
homotypic  to  distinguish  it  from  the  usual  (typical  mitoses  in  which  there  are  no  premature 
divisions  of  the  chromosomes.  All  figures  after  Mottier. 

to  this  phenomenon.     (See  account  of  spore  mother  cell  in  Sec- 
tion III. 

Anaphase. —  Anaphase  begins  with  the  separation  of  the 
daughter  chromosomes  at  the  nuclear  plate  (Fig.  6 )  and  ends 
with  the  gathering  of  these  structures  at  the  poles  of  the 
spindle  preparatory  to  the  organization  of  the  daughter  nuclei. 
As  the  chromosomes  move  towards  the  poles  the  fibers  of  the 
central  spindle  stand  out  sharply  (see  Fig.  6  b}.  If  a  cell  wall 
is  to  be  formed  between  the  daughter  nuclei  one  may  expect  to 
find  these  fibers  thickening  in  the  equatorial  region  of  the 


No.  450.] 


STUDIES   ON   THE    PLANT  CELL. 


447 


spindle  where  the  nuclear  plate  formerly  lay.  Such  thickenings 
are  granular  accumulations  formed  by  the  contraction  of  the 
central  spindle  fibers  and  mark  the  beginnings  of  the  cell  -plate 
(Fig.  8  d}  that  afterwards  gives  rise  to  the  cell  wall.  When 
the  daughter  chromosomes  reach  the  poles  of  the  spindle  they 
generally  lie  in  a  region  of  granular  kinoplasm  which  results  in 
part  from  the  contraction  of  spindle  fibers  and  in  some  cases 
from  the  breaking  down  of  organized  centrospheres  (e.  g.,  Coral- 
lina,  Pellia,  Fucus,  etc.).  The  daughter  nucleus  at  this  time 


FIG.  7. —  Telophase  of  Mitosis,  spore  mother-cell  of  Passiflora  coerulea.  a,  very  lateanaphase  ; 
the  daughter  chromosomes  are  collected  at  the  poles  of  the  spindle,  b,  the  commence- 
ment of  telophase  ;  the  chromosomes  have  fused  together  and  the  daughter  nucleus  is 
represented  by  an  irregularly  shaped  mass  of  chromatin.  c,  the  presence  of  small  lacunae 
within  the  mass  of  chromatin  indicates  the  accumulation  of  nuclear  sap  in  vacuoles.  d,  an 
increased  amount  of  nuclear  sap,  still  held  however  within  the  mass  of  chromatin,  and 
consequent  enlargement  of  the  vacuole  destined  to  become  the  nuclear  cavity,  e,  the 
chromatin  has  begun  to  break  up  into  small  masses  so  that  it  no  longer  holds  the  nuclear 
sap  which  has  established  contact  with  the  cytoplasm  and  is  forming  the  nuclear  plasma 
membrane,  f,  nuclear  sap  in  contact  on  all  sides  with  the  cytoplasm  and  a  complete 
nuclear  membrane  clearly  established;  chromatin  is  very  much  broken  up  and  two  nucleoli 
(n)  have  been  formed,  g,  the  resting  nucleus  with  chromatin  distributed  in  small  masses 
connected  by  a  network  of  linin  threads;  a  nucleolus  (n)  is  shown  ;  the  zone  outside  the 
nuclear  membrane  is  kinoplasm  and  its  appearance  indicates  the  approach  of  the  second 
mitosis  in  the  pollen  mother-cell.  All  figures  after  Lawson. 

(Fig.  7  a,  b]  is  in  its  simplest  terms,  as  explained  in  Section  I, 
a  group  of  chromosomes  surrounded  by  granular  kinoplasm  and 
without  the  nucleolus,  linin  network  or  the  vacuole  which  later 
contains  the  nuclear  sap. 

Telophase. — Telophase   is    the  closing  period  of  mitosis  and 
completes  the  organization  of  the  daughter  nuclei  (see  Fig.  7). 


448  THE  AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

The  chromosomes  come  to  lie  in  a  vacuole  (Fig.  7  c,  d,  e)  con- 
taining nuclear  sap  and  later  the  chromatin  becomes  distributed 
over  a  linin  network  and  one  or  more  nucleoli  develop  (Fig. 
7  f>  <£")•  As  was  stated  in  Section  I,  the  nuclear  membrane 
probably  represents  the  reaction  of  the  granular  kinoplasm  to  a 
fluid  secretion  around  the  chromosomes  which  becomes  the 
nuclear  sap  (La wson,  :O3a).  However,  the  nuclear  membrane 
is  generally  a  definitely  organized  film,  much  more  sharply 
defined  than  vacuolar  membranes.  The  development  of  the 
linin  network  is  not  well  understood.  It  is  readily  seen  that 
the  chromosomes  become  joined  end  to  end  and  sometimes  elon- 
gate. The  amount  of  chromatin  diminishes  as  the  linin  substance 
appears,  but  it  is  not  certain  whether  the  chromatin  is  changed 
directly  into  linin,  or  whether  the  latter  substance  is  a  secretion: 
The  best  evidence  rather  favors  the  former  view.  Nucleoli  are 
also  believed  to  hold  a  very  close  chemical  relation  to  chromatin. 

It  is  uncertain  whether  or  not  the  chromosomes  lose  their 
organic  identity  in  the  daughter  nuclei.  Investigations  on  this 
problem  are  surrounded  by  many  difficulties.  It  has  been 
claimed  by  Guignard  ('99)  for  Naias  and  Strasburger  (:  oo)  for 
several  forms  that  the  chromosomes  may  be  followed  with  cer- 
tainty through  the  period  between  the  first  and  second  mitosis 
in  the  spore  mother  cell.  But  other  investigators  have  not  been 
able  to  trace  the  chromosomes  after  telophase  and  are  inclined 
to  believe  that  the  chromosome  completely  loses  its  identity  in 
the  resting  nucleus.  One  of  the  last  investigations  of  Lilium 
(Mottier,  :  03)  argues  strongly  for  the  latter  view,  and  all  who 
have  followed  nuclei  from  one  mitosis  into  another  know  that 
the  resting  nucleus  with  its  linin  network  and  the  granular 
chromatin  present  conditions  that  generally  make  the  recognition 
of  chromosomes  impossible  with  the  instruments  and  technique 
at  our  command,  but  this  does  not  prove  that  they  may  not  be 
present. 

The  theory  of  the  permanence  of  the  chromosome  has  met 
with  much  favor  because  it  is  argued  that  otherwise  how  could 
the  number  be  maintained  so  regularly  through  immense  num- 
bers of  mitoses.  But  it  can  hardly  be  said  that  the  doctrine  is 
established.  It  has  also  found  favor  because  all  the  events  of 


No.  450.]  STUDIES   ON   THE   PLANT  CELL.  449 

mitosis  emphasize  the  importance  of  the  chromosomes  which 
are  really  the  only  enduring  structures  in  the  nucleus  and  have 
led  to  their  being  considered  as  the  probable  bearers  of— heredi- 
tary qualities. 

3.  The  Dynamics  of  Nuclear  Division. 

Mitotic  phenomena  in  certain  plant  cells  present  evidence  that 
has  very  direct  bearing  on  some  of  the  theories  that  deal  with 
mechanical  and  dynamical  explanations  of  nuclear  division.  The 
methods  of  spindle  formation  and  the  various  forms  of  kinoplas- 
mic  structures  (centrosomes,  centrospheres  and  kinoplasmic 
caps)  which  generally  in  plants  seem  not  to  be  permanent 
organs  of  the  cells  all  tend  to  support  Strasburger's  conception 
of  kinoplasm,  which  is  an  outgrowth  and  application  to  plants  of 
Boveri's  well  known  theory  of  archoplasm. 

The  centrosome  theory  is  supported  by  very  few  investiga- 
tions in  Botany,  the  most  notable  being  that  of  Swingle  ('97), 
for  Stypocaulon,  who  believes  that  the  centrosome  divides  with 
the  aster  and  is  maintained  as  a  permanent  organ  throughout 
successive  cell  divisions.  Other  examples  of  similar  conditions 
may  be  found  among  the  thallophytes  which,  after  all,  have 
received  very  little  attention,  and  such  types  as  Dictyota  and 
the  diatoms  offer  excellent  subjects  for  studies  covering  a 
series  of  cell  divisions.  But  in  contrast  to  Stypocaulon  it  should 
be  noted  that  the  conspicuous  centrospheres  of  Fucus  and  Cor- 
allina  disappear  with  each  mitosis  to  be  formed  anew,  and  the 
same  conditions  obtain  in  the  germinating  spores  of  liverworts 
(Pellia).  There  seems  to  be  no  place  for  the  centrosome  in 
spindle  formation  as  presented  in  the  spore  mother  cells  of  all 
groups  above  the  thallophytes  (see  Sec.  III).  Neither  does 
mitosis  in  the  vegetative  tissues  of  these  groups,  characterized 
as  it  is  by  the  presence  of  kinoplasmic  caps,  conform  to  the 
program  of  the  centrosome  theory. 

The  morphological  manifestations  of  kinoplasm  are  so  various 
that  we  are  driven  to  a  very  general  conception  of  its  organiza- 
tion. Kinoplasm  runs  through  cycles  in  which  the  structure 
passes  from  a  granular  condition  to  a  fibrillar  and  then  back  again 


450  THE   AMERICAN  NATURALIST.   [VOL.  XXXV II I. 

to  the  granular  state.  By  the  granular  state  we  mean  one  in 
which  no  fibrillae  seem  to  be  present,  but  instead  the  microsomata 
are  densely  and  homogeneously  massed.  It  is  possible  that  such 
microsomata  form  a  closely  packed  network,  but  no  such  struc- 
ture is  visible  under  the  microscope.  The  first  appearance  of 
kinoplasm  at  prophase  of  mitosis  is  frequently  the  granular 
condition.  This  state  is  illustrated  by  such  accumulations  as 
centrospheres  and  kinoplasmic  caps  and  by  the  granular  zone 
that  has  been  reported  around  the  nuclei  of  some  spore  mother 
cells. 

Granular  kinoplasm  becomes  fibrillar  probably  by  the  arrange- 
ment of  the  microsomata  into  a  reticulum  from  which  fibers 
extend  freely  into  the  surrounding  cytoplasm.  These  fibers 
undoubtedly  elongate  during  prophase,  extending  in  various 
directions.  Some  press  against  the  nuclear  membrane  and  when 
this  breaks  down  grow  rapidly  into  the  nuclear  cavity.  Of  these 
a  portion  extend  from  pole  to  pole  and  form  the  central  spindle. 
Others  attach  themselves  to  the  chromosomes  and  lie  either 
among  the  central  fibers  or  somewhat  outside  of  the  spindle 
(mantle  fibers).  Still  others  may  extend  freely  into  the  cyto- 
plasm as  astral  rays  from  the  pole  of  the  spindle,  a  very  com- 
mon condition  when  centrosomes  or  centrospheres  are  present. 
A  contraction  of  the  fibrillae,  beginning  with  metaphase,  is  just 
as  characteristic  of  mitosis  as  their  elongation  during  prophase. 
The  fibers  attached  to  the  chromosomes  draw  the  latter  to  the 
poles  of  the  spindle.  The  central  fibers  in  higher  plants  draw 
away  from  the  poles  and  give  their  substance  to  the  cell  plate. 
The  substance  of  contracted  mantle  fibers,  with  other  kinoplasm 
at  the  poles  of  the  spindle,  probably  become  distributed  around 
the  group  of  daughter  chromosomes  so  that  they  finally  lie  sur- 
rounded by  a  sphere  of  kinoplasm. 

It  does  not  seem  as  if  we  knew  much  more  about  the  struc- 
ture and  activities  of  kinoplasm  during  mitosis  than  is  indicated 
in  this  cycle  of  change  from  a  granular  condition  through  a 
fibrillar  state  back  to  the  granular  condition,  with  a  period  when 
the  fibers  elongate  and  another  when  they  contract.  This  with 
few  exceptions  is  the  history  for  every  mitosis.  The  exceptions 
deal  with  peculiar  conditions  or  structures.  Thus,  for  example, 


No.  450.]  STUDIES   ON   THE   PLANT  CELL.  45  I 

the  astral  rays  of  the  centrospheres  in  the  ascus  instead  of  con- 
tracting to  a  center  or  disappearing  in  the  cytoplasm  after  the 
last  mitosis  grow  around  the  nucleus  and  cut  out  a  portion  of 
the  cytoplasm  to  form  the  spores,  thus  contributing  their  sub- 
stance to  a  plasma  membrane. 

There  is  little  doubt  that  kinoplasmic  fibrillae  actually  exist  as 
structural  elements  in  the  protoplasm.  Their  growth  and  move- 
ment in  the  cytoplasm  and  nuclear  cavity,  their  multiplication 
and  shifting  arrangements  as  the  spindle  develops,  and  their 
contraction  to  the  poles  of  the  spindle  or  to  a  cell  plate  give 
these  fibers  an  individuality  that  cannot  be  explained  on  the 
theory  that  they  merely  represent  lines  of  force  or  paths  of 
dynamic  stimuli.  They  apparently  perform  all  the  activities 
mentioned  above  by  virtue  of  their  own  structural  organization 
which  is  that  of  rows  of  microsomata  and  in  this  organization 
resemble  and  are  probably  closely  related  to  cilia.  There  is  an 
excellent  discussion  of  this  subject  by  Allen,  :  03,  p.  302,  etc. 

Some  authors  believe  that  there  is  a  streaming  movement  in 
the  astral  rays  (Chamberlain,  :  03,  for  Pellia)  either  towards  or 
away  from  the  pole  of  the  spindle.  This  view  is  founded  on  the 
granular  appearance  of  the  radiations  which  are  sometimes  very 
thick  in  Pellia  and  enlarge  at  the  points  where  they  join  the 
centrospheres  or  the  outer  plasma  membrane.  It  is  not  alto- 
gether clear  that  the  larger  of  these  structures  are  quite  the 
same  as  spindle  fibers  since  they  seem  to  be  actually  strands  of 
cytoplasm  rather  than  fibrillae. 

It  is  probably  safe  to  assume  that  the  forms  which  kinoplasm 
takes  have  relation  to  dynamic  activities,  but  it  is  not  easy  to 
define  these.  Thus  centrosomes,  centrospheres  and  kinoplasmic 
caps  may  well  be  the  centers  from  which  dynamic  stimuli  extend, 
and  they  may  be  the  focal  points  of  other  energies.  These 
problems  have  been  very  little  investigated  among  plants.  It  is 
obvious  that  differentiated  regions  of  kinoplasm  have  important 
physical  relations  to  other  portions  of  the  protoplasm,  one  of  the 
most  important  being  the  anchorage  which  they  give  to  fibrillae, 
thereby  largely  governing  the  direction  of  such  strains  as  come 
about  through  the  contraction  of  these  structures  in  the  later 
periods  of  mitosis. 


452  THE   AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

But  the  essential  characteristics  of  kinoplasm  stand  out  sharply 
from  whatever  point  the  phenomena  of  mitosis  is  viewed,  and  in 
this  protoplasm  with  its  power  of  forming  contractile  fibers  is 
vested  some  of  the  most  conspicuous  activities  of  nuclear  division 
as  well  as  the  important  powers  given  plasma  membranes  in 
relation  to  the  segmentation  of  protoplasm  to  be  considered 
presently. 

The  dynamic  activities  concerned  with  the  spindle  present  only 
half  the  story  of  mitosis.  The  other  important  events  occur 
inside  of  the  nucleus.  One  of  these  is  the  dissolution  of  a  por- 
tion or  the  whole  of  the  nucleolus  which  takes  place  as  the 
spindle  develops  and  we  have  already  given  the  views  of  Stras- 
burger  ('95  and  :  oo),  supported  by  the  studies  of  other  investi- 
gators, that  its  substance  in  certain  instances  furnishes  material 
for  the  development  of  the  spindle.  But  the  chief  events  in  the 
interior  of  the  nucleus  deal  with  the  accumulation  of  chromatin 
on  the  spirem  thread  which  with  the  disappearance  of  the  linin 
indicates  that  the  latter  substance  may  become  converted  into 
the  former.  The  splitting  of  the  spirem  ribbon  longitudinally  is 
of  the  utmost  significance  for  thereby  is  made  possible  an  exact 
and  homogeneous  distribution  of  the  chromatic  material  in  the 
nucleus.  We  do  not  know  how  the  spirem  ribbon  splits  nor 
have  we  as  yet  any  evidence  of  the  origin  and  evolution  of  this 
peculiar  activity. 

(b)   Segmentation  of  the  Protoplasm. 

Mitosis  in  the  uninucleate  cells  of  plants  is  generally  followed 
by  immediate  cell  division,  which  takes  place  in  groups  above 
the  thallophytes  through  the  formation  and  cleavage  of  the  cell 
plate  in  the  equatorial  region  of  the  spindle  between  the  daughter 
nuclei.  Among  thallophytes,  as  so  far  studied,  cell  division  is 
chiefly  through  cleavage  by  constriction.  There  are  forms  among 
the  thallophytes  and  also  in  the  spermatophytes  whose  nuclei 
gather  about  themselves  a  portion  of  the  cytoplasm,  wherein 
they  lie,  which  becomes  cut  out  of  the  general  mass  by  a  cell 
wall.  This  is  free  cell  formation. 

Multinucleate  masses  of  protoplasm,  such  as  plasmodia  and 


No.  450.]  STUDIES   ON    THE   PLANT  CELL.  453 

portions  of  coenocytes,  generally  divide  extensively  at  repro- 
ductive periods  and  always  through  cleavage  by  constriction  with, 
however,  the  frequent  cooperation  of  vacuoles  which  heip~to  cut 
the  protoplasm  in  the  same  manner  as  the  cleavage  furrows. 
Cleavage  by  constriction  is  undoubtedly  the  most  primitive  type ; 
free  cell  formation  and  cleavage  by  cell  plates  being  special  and 
very  highly  developed  protoplasmic  activities. 

i .   Cleavage  by  Constriction. 

A  simple  example  of  cleavage  by  constriction  is  presented  by 
such  an  alga  as  Cladophora.  The  process  consists  in  the  build- 
ing out  of  a  ring  of  cellulose  from  the  side  wall  into  the  cell 
cavity.  The  outer  plasma  membrane  forms  a  fold,  thus  placing 
the  two  surfaces  opposite  one  another  (see  Fig.  8  a),  and  the 
wall  is  laid  down  between  these.  Spirogyra  forms  its  wall  in 
precisely  the  same  manner  as  Cladophora  with  this  peculiarity, 
that  the  new  wall  finally  cuts  through  the  protoplasmic  strands 
that  connect  the  daughter  nuclei.  These  strands  are  said  to  con- 
tain spindle  fibers  (Van  Wisselingh,  :  02)  which  may  contribute  to 
the  plasma  membranes  forming  the  cell  wall,  as  it  is  completed. 
Another  illustration  of  cleavage  by  constriction  is  presented  in  the 
formation  of  gametes  of  moulds  (Sporodinia)  and  the  abstric- 
tion  of  conidia  (Erysipheae),  both  processes  having  been  studied 
by  Harper,  '99,  p.  506.  In  these  cases  a  cleavage  furrow  pro- 
ceeds from  the  surface  inward  and  divides  the  protoplasm.  The 
partition  wall  of  cellulose  is  formed  later  between  the  two  free 
plasma  surfaces.  The  only  differences  between  the  processes 
above  described  are  that  in  the  first  forms  the  cleavage  proceeds 
more  slowly  and  the  wall  follows  the  furrow  as  it  progresses  in 
the  interior  of  the  cell,  while  in  the  latter  types  cleavage  is  com- 
plete before  the  plasma  membranes  develop  the  wall.  Cell 
division  in  the  red  Algae  (Rhodophyceae)  is  also  a  process  of 
constriction  similar  to  Cladophora,  but  the  wall  is  not  generally 
formed  entirely  across  the  filament  so  that  adjacent  cells  remain 
connected  by  thick  strands  of  protoplasm. 

These  processes  become  much  more  complicated  when  large 
masses  of  multinucleate  protoplasm  are  divided  up  into  many 


454  THE   AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

smaller  bodies  as  during  spore  formation  among  the  Myxomy- 
cetes  and  Mucorales.  Very  complete  studies  have  been  made  of 
these  conditions  by  Harper,  '99  and  :ooa.  In  the  slime  mould 
(Fuligo)  cleavage  begins  by  furrows  on  the  external  surface 
which  "  cut  down  at  all  angles  into  the  homogeneous  proto- 
plasm." The  direction  of  the  cleavage  furrows  is  further  com- 
plicated by  the  fact  that  many  of  them  start  from  the  bottom 
and  sides  of  deep  folds.  All  of  the  furrows  may  bend  and 
secondary  cleavage  planes  strike  off  from  them  which  in  time 
unite  with  one  another  until  the  protoplasm  is  divided  progres- 
sively into  very  many  small  masses  (see  Fig.  8  b~)  that  finally 
round  themselves  off  and  secrete  walls,  becoming  spores,  some- 
times with  one  nucleus  and  sometimes  with  several. 

Cleavage  in  the  sporangium  of  Synchytrium  and  the  moulds, 
as  described  by  Harper,  '99,  is  in  general  similar  to  that  in  the 
plasmodium  with,  however,  the  additional  feature  that  lines  or 
planes  of  vacuoles  are  often  utilized  to  assist  a  cleavage  furrow 
in  effecting  the  segmentation  of  the  protoplasm.  The  separa- 
tion of  the  spore  plasm  of  the  sporangium  of  Pilobolus  from  the 
filament  below  begins  with  a  cleavage  furrow  from  the  exterior ; 
but  this  furrow  follows  and  makes  use  of  a  curved  plane  of 
flattened  vacuoles  with  the  result  that  a  dome  shaped  cleft  is 
developed  and  two  plasma  membranes  are  presented  face  to  face, 
which  form  the  columella  wall  between  them.  The  segmenta- 
tion of  the  spore  plasm  in  Pilobolus  is  affected  somewhat 
similarly  through  the  cooperation  of  cleavage  furrows  from 
the  exterior  with  vacuoles  which  cut  into  the  protoplasm  at 
various  angles  to  meet  one  another  and  the  cleavage  furrows. 
The  bodies  first  formed  in  the  sporangium  of  Pilobolus  are  not 
the  final  spores.  Harper  suggests  that  they  may  correspond  to 
the  zoospores  of  Saprolegnia.  They  are  generally  uninucleate 
and  begin  immediately  a  period  of  growth  within  the  sporangium 
characterized  by  extensive  nuclear  multiplication  and  several 
divisions  of  the  protoplasmic  body  by  constriction. 

Harper  finds  that  the  spore  plasm  of  Sporodinia  is  separated 
from  the  filament  below  by  a  dome-shaped  plane  of  flattened 
vacuoles  which  fuse  together  and,  unlike  Pilobolus,  cut  their  way 
to  the  surface  of  the  sporangium.  Thus  the  cleavage  is  deter- 


No.  450.]  STUDIES   ON   THE   PLANT  CELL.  455 

mined  entirely  by  the  activity  of  vacuoles.  Spore  formation, 
however,  is  accomplished  by  cleavage  furrows  which  progress 
from  the  exterior  inwards  and,  without  the  aid  of  conspicuous 
vacuoles,  cut  out  multinucleate  masses  of  protoplasm  which 
become  the  spores. 

Dean  Swingle  (:  03)  has  extended  the  studies  of  Harper  on 
spore  formation  in  the  molds  to  Rhizopus  and  Phycomyces.  He 
confirms  Harper's  account  of  the  general  processes  of  cleavage 
by  furrows  cooperating  with  vacuoles,  and  notes  the  following 
characteristics  in  the  types  studied.  In  Rhizopus  the  position 
of  the  columella  is  determined  by  a  dome-shaped  series  of  flat- 
tened vacuoles  which  fuse  and  meet  a  cleft  that  extends  upward 
from  the  outer  plasma  membrane  at  the  base  of  the  sporangium. 
The  spores  are  formed  in  Rhizopus  by  branching  systems  of 
curved  furrows  that  cut  the  protoplasm  into  multinucleate  masses, 
and  in  Phycomyces  by  angular  vacuoles  that  develop  into  furrows 
which  extend  in  various  directions  and  unite  with  one  another 
and  with  clefts  from  the  region  of  the  columella. 

Other  excellent  illustrations  of  cleavage  by  constriction  are 
presented  in  the  sporangia  of  such  types  as  Hydrodictyon,  Clado- 
phora  and  Saprolegnia.  Timberlake  (:  02)  has  given  an  account 
of  Hydrodictyon,  and  the  events  are  also  fairly  well  understood 
for  Saprolegnia.  Segmentation  begins  in  Hydrodictyon  by  the 
development  of  cleavage  furrows  in  the  outer  plasma  membrane, 
which  cut  into  the  protoplasmic  layer  at  right  angles  to  the 
surface  and  meet  similar  furrows  that  make  their  way  from  the 
large  central  vacuole  outward.  These  cleavage  planes  spread  lat- 
erally, uniting  with  one  another,  until  the  protoplasm  is  all 
divided  into  uninucleate  masses  which  become  the  zoospores 
(Fig.  8  c).  In  Saprolegnia  (see  Davis,  103,  for  general  account) 
conspicuous  cleavage  furrows  develop  from  the  central  vacuole 
and  make  their  way  to  the  exterior,  finally  breaking  through  the 
outer  plasma  membrane.  When  this  takes  place  there  is  an 
immediate  escape  of  cell  sap,  which  was  under  pressure,  and  a 
shrinkage  of  the  sporangium  so  that  the  zoospore  origins  appear 
to  fuse,  but  this  is  not  really  the  case,  for  cleavage  is  continued 
and  the  zoospores  soon  separate. 

A  physiological  explanation  of  cleavage  by  constriction  must 


456  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

consider  two  sets  of  factors.  There  is  an  evident  contraction  of 
the  protoplasm  in  many  examples  because  water  is  given  off. 
The  shrinkage  of  the  surface  would  undoubtedly  form  furrows, 
but,  as  Harper  has  pointed  out,  these  furrows  do  not  develop  in 
an  accidental  manner.  Non-nucleated  masses  of  protoplasm  are 
never  separated  from  the  nucleated,  but  the  segmentation  pro- 
ceeds after  a  system  by  which  the  final  products  contain  only 
one  nucleus  or  at  most  a  limited  number.  So  it  is  probable  that 
the  nuclei  are  the  ultimate  centers  controlling  the  segmentation 
which  at  its  commencement  may  be  quite  irregular.  This 
explanation  of  sporogenesis  in  the  plasmodium  and  the  spo- 
rangium is  not  altogether  satisfactory  for  the  cell  division  of 
Cladophora,  the  abstriction  of  conidia  or  the  development  of  the 
gametes  of  a  mould.  In  these  examples  the  cleavage  begins  at 
definite  regions  of  the  plasma  membrane,  so  that  the  stimulus 
must  be  local,  and  the  direction  of  the  plane  has  a  definite 
relation  to  the  axis  of  the  plant. 

It  is  important  to  note  (see  Harper,  :  oo,  p.  240-249)  how 
inadequate  are  some  of  the  well-known  theories  of  the  segmen- 
tation of  protoplasm  as  explanations  of  cleavage  by  constriction. 
Hofmeister's  law  ('67)  that  cell  division  is  across  the  axis  of 
growth  obviously  cannot  be  applied  to  the  irregular  segmentation 
in  the  plasmodium  and  sporangium,  nor  is  Sachs'  well-known  law 
of  growth  in  vegetative  points  adequate.  Sachs,  '94,  and  in  the 
Lectures  on  the  Physiology  of  Plants,  chap.  XXVII,  conceives 
a  growing  point  of  a  higher  plant  or  an  embryonic  structure  as  a 
mass  of  protoplasm  whose  cell  walls  are  determined  by  principles 
of  rectangular  intersection  of  perpendicular  planes.  The  outer 
form  of  the  structure  determines  the  angles  of  periclines  and 
anticlines  and  the  transversals  conform  to  these.  There  is  not 
the  slightest  hint  of  such  an  order  in  the  distribution  of  cleavage 
planes  in  the  multinucleate  masses  of  protoplasm  just  described 
and  Sachs'  law  in  so  far  fails  of  general  application  whether  or 
not  it  be  satisfactory  for  the  conditions  with  which  he  especially 
deals.  There  are  also  explanations  of  cell  division,  applicable  to 
the  tissues  of  many  higher  organisms,  based  on  the  position  of 
the  nuclear  figure  in  the  cell,  which  determines  the  position  of 
the  cell  plate  but  these  theories  cannot  handle  the  events  in  the 


No.  450.]  STUDIES   ON   THE  PLANT  CELL.  457 

plasmodium  or  sporangium  where  the  cleavage  planes  are  formed 
without  regard  to  the  time  of  nuclear  division  or  the  position  of 
mitotic  figures. 

2.    Cleavage  by  Cell   Plates. 

Cleavage  of  the  protoplasm  by  means  of  the  cell  plate  is 
almost  universal  in  cell  division  of  plants  above  the  thallophytes. 
It  is  one  of  the  peculiarities  of  plant  cells,  having  been  found  in 
comparatively  f e w Animals  and  there  represented  rather  imper- 
fectly by  the  so-called^  mid-body.  The  general  events  of  the 
process  have  been  known  since  Treubs'  studies  of  1878,  and 
were  clearly  described  by  Strasburger  in  1880.  Timberlake, 
:  oo,  in  a  recent  paper  gives  an  historical  review  of  the  subject. 

When,  after  the  metaphase  of  mitosis,  the  two  sets  of  daugh- 
ter chromosomes  separate  from  one  another  there  is  left  between 
them  the  spindle,  made  up  of  the  central  fibers.  The  first 
appearance  of  the  cell  plate  is  a  line  of  granules  in  the  equatorial 
region  of  this  spindle  where  the  nuclear  plate  formerly  lay. 
But  several  important  events  proceed  this  condition.  The  con- 
necting central  fibers  begin  to  thicken,  first  near  the  daughter 
nuclei,  and  then  gradually  towards  the  equatorial  region  of  the 
spindle.  The  number  of  fibers  may  increase  greatly,  probably 
by  the  separation  of  bundles  of  fibrillae  composing  the  spindle 
into  independent  elements  (Timberlake,  :  oo,  p.  94).  But  there 
is  evidence  that  new  fibrillae  are  sometimes  formed  from  the 
vicinity  of  the  daughter  nuclei,  some  of  which  may  enter  the 
spindle  and  cooperate  with  the  connecting  fibers.  In  certain 
forms  (e.  g.  Allium)  there  is' an  accumulation  of  a  stainable  sub- 
stance between  the  connecting  fibers  in  the  equatorial  region  of 
the  spindle.  The  reaction  of  this  substance  to  stains  indicates 
a  carbohydrate  composition. 

The  cell  plate  really  begins  with  the  thickening  of  the  con- 
necting fibers  in  the  equatorial  plane  of  the  spindle.  In  some 
forms  these  thickenings  are  elongated  bodies,  in  others  mere 
granules.  The  earlier  writers  (Treub,  '78,  Zacharias,  '88)  did 
not  believe  that  they  came  from  the  spindle  fibers,  but  there 
seems  to  be  now  no  doubt  of  their  origin  from  these  elements, 


458 


THE   AMERICAN  NATURALIST.  [VOL.  XXXVIII. 


which  contract  and  thicken  as  the  plate  develops.  The  bodies 
composing  the  cell  plate  finally  lie  in  a  plane  extending  the 
entire  width  of  the  spindle  (Fig.  8  d)  and  they  then  broaden 
and  come  in  contact  with  one  another  to  form  a  continuous 
membrane,  which,  as  has  been  said,  may  lie  in  a  matrix  of  car- 
bohydrate material.  The  cell  plate  grows  rapidly  as  the  central 
spindle  fibers  shorten  and  contribute  their  substance  to  the 
structure.  During  this  contraction  the  surrounding  cytoplasm 


FIG.  8. —  Segmentation  of  the  Protoplasm,  a,  b,  c,  cleavage  by  constriction,  d,  cleavage  by 
cell  plate,  e,  f,  g,  free  Cell  Formation.  «,  cell  division  in  Cladophora.  b,  cleavage  of 
spore  plasm  in  Fuligo.  c,  spore  formation  in  Hydrodictyon.  d,  first  division  of  spore 
mother-cell  in  Pellia.  e,  spore  formation  in  ascus,  i  and  2  (Erysiphse)  astral  fibers  cutting 
out  cytoplasm  around  nuclei,  3  portion  of  ascus  with  developing  spores  (Lachnea).  f, 
obgonium  of  Albugo,  egg  surrounded  by  membrane  pierced  by  antheridial  tube,  ccenocen- 
trum  and  female  gamete  nucleus  within,  g,  egg  of  Ephedra  with  four  embryo  cells.  After 
Strasburger  Harper  and  Timberiake. 

enters  the  region  between  the  barrel  shaped  group  of  fibers  and 
the  daughter  nuclei  (Fig.  8  d}.  It  is  probable  that  the  cell  plate 
is  composed  entirely  of  the  substance  of  spindle  fibers  and  in 
consequence  is  kinoplasmic  in  character.  The  cell  plate  widens 
with  the  accretion  of  material  from  the  central  spindle,  which  in 
some  cases  is  assisted  by  the  radiating  fibers  that,  lying  outside 
of  the  spindle,  contract  and  add  their  material  to  the  edge  of  the 
plate.  The  cell  plate  thus  extends  laterally  and  finally  reaches 


No.  450.]  STUDIES   ON   THE  PLANT  CELL.  459 

the  neighboring  cell  walls,  fusing  with  the  outer  plasma  mem- 
brane. There  are  certain  mitoses,  as  in  some  spore  mother  cells 
and  in  the  embryo  sac  (see  Section  III)  where  the  c^l  -plates 
are  absorbed  into  the  cytoplasm  leaving  the' original  cell  with 
two  or  more  nuclei  and  without  partition  walls.  It  is  uncertain 
whether  the  edge  of  the  plate  is  ever  extended  by  the  develop- 
ment of  additional  peripheral  fibrillae  (Timberlake,  :  oo,  p.  161) 
from  the  daughter  nuclei. 

Cell  division  is  accomplished  by  the  splitting  of  the  cell  plate 
(Strasburger,  '98)  into  two  plasma  membranes.  The  division 
generally  begins  in  the  center  and  the  cleft  progresses  towards 
the  periphery  until  it  reaches  the  cell  wall.  During  the  process 
the  thickened  rod  shaped  portions  of  the  spindle  fibers  are  pulled 
apart.  There  are  thus  left  two  kinoplasmic  membranes  opposite 
one  another  and  continuous  with  the  outer  plasma  membrane 
surrounding  the  daughter  cells.  The  cause  of  this  cleavage  is 
not  apparent,  but  there  are  reasons  for  believing  that  the  split 
is  essentially  a  thin  vacuole  which,  starting  near  the  center,  cuts 
its  way  through  the  cell  plate  to  the  periphery  after  a  manner 
very  similar  to  the  behavior  of  vacuoles  during  the  cleavage  of 
the  plasmodium  and  in  the  sporangia  of  certain  moulds.  And 
there  may  be  shown  in  this  activity  a  relationship  of  cleavage  by 
cell  plate  to  some  of  the  events  of  cleavage  by  constriction. 
After  division  is  complete  there  follows  the  formation  of  a  cell 
wall  between  the  two  cell  surfaces  after  the  method  usual  to 
plasma  membranes. 

The  new  cell  wall  generally  begins  in  the  oldest  portion  of  the 
cell  plate  where  the  cleft  first  appeared  and  is  gradually  built 
out  peripherally  until  it  reaches  the  side  walls.  The  first  indica- 
tion of  the  wall  is  the  appearance  in  the  cleft  of  a  stainable 
carbohydrate  substance  which  resembles  the  material  that  was 
primarily  present  between  the  fibers  of  the  central  spindle  and 
which  disappears  with  the  formation  of  the  cell  plate.  This 
material  is  probably  the  basis  of  the  first  deposits  on  the  surface 
of  the  two  plasma  membranes,  but  the  nature  of  the  final  sub- 
stance is  exceedingly  various.  A  cell  wall  may  be  formed  that 
is  homogeneous  throughout  but  often  the  thickened  wall  presents 
three  regions,  two  layers  of  a  cellulose  basis  formed  by  the 


460  THE  AMERICAN  NATURALIST.  [VOL.  XXXVI II. 

respective  plasma  membranes  and  between  them  the  so-called 
middle  lamella. 

The  middle  lamella  has  been  the  subject  of  much  discussion. 
It  is  not  the  remains  of  the  cell  plate  as  was  once  supposed. 
Neither  is  it  exactly  a  cement  between  two  cell  walls.  Its  his- 
tory is  undoubtedly  various,  for  the  composition  shows  much 
plasticity.  The  origin  of  the  middle  lamella  at  the  surface  of 
a  plasma  membrane  indicates  a  morphology  similar  to  a  cell  wall, 
but  the  substance,  pectic  in  character,  shows  transformations  far 
removed  from  the  cellulose  compounds  that  are  formed  later  and 
which  give  thickness  to  the  cell  wall.  Allen  (:oi)  discusses  the 
subject  in  detail. 

The  origin  of  the  cell  plate  is  a  subject  of  interest  which  will 
be  further  discussed  in  Section  VI.  There  are  some  types,  espe- 
cially among  the  thallophytes,  where  a  cell  plate  is  present,  but 
apparently  in  a  somewhat  undeveloped  and  rudimentary  condi- 
tion. These  forms  suggest  transitional  conditions  between  cleav- 
age by  constriction  with  the  aid  of  vacuoles,  so  general  among 
the  thallophytes,  and  cleavage  by  the  cell  plate,  characteristic  of 
higher  groups.  The  most  interesting  examples  are  Anthoceros, 
Chara,  Basidiobolus,  Pelvetia,  Fucus,  and  Sphacelaria. 

Cell  plates  are  formed  with  each  of  the  two  successive  mitoses 
in  the  spore  mother  cell  of  Anthoceros  (Van  Hook,  :  oo ;  Davis, 
:oi,  p.  158),  but  the  structure  in  some  species  is  exceedingly 
small  (e.  g.,  A.  Icevis}  and  can  scarcely  extend  more  than  one- 
tenth  of  the  distance  across  the  cell.  It  is  larger  in  other  forms, 
as  in  the  one  studied  by  Van  Hook ;  but  even  there  the  nuclear 
figure  of  the  second  mitosis  is  only  one-third  of  the  width  of  the 
cell.  The  protoplasm  divides  simultaneously  in  the  four  spores 
with  the  characteristic  arrangement.  If  this  division  were  deter- 
mined entirely  by  cell  plates  there  would  be  required  an  exten- 
sive development  of  fibrillae,  of  which  there  is  no  evidence  in  the 
cell.  But  their  place  seems  to.be  taken  by  numerous  delicate 
strands  of  cytoplasm  which  connect  the  four  protoplasmic  masses, 
each  of  which  contains  a  large  chromatophore  and  an  accom- 
panying nucleus.  A  film  is  formed  in  the  intermediate  region, 
and  this  marks  the  position  of  the  cell  wall.  It  is,  of  course, 
quite  certain  that  the  two  cell  plates  of  the  second  mitosis  are 


No.  450.]  STUDIES   ON   THE   PLANT  CELL.  461 

a  part  of  this  membrane  and  may  start  its  development,  but  the 
final  structure  must  contain  very  much  more  material  than  could 
possibly  be  contributed  by  the  sparsely  developed  spindle  fibers . 
Thus,  although  the  splitting  of  the  cell  plate  may  start  the  proc- 
ess of  segmentation,  its  final  course  and  end  is  probably  deter- 
mined by  cleavage  through  vacuoles,  thus  utilizing  a  method 
characteristic  of  the  thallophytes. 

Chara  appears  to  have  a  fairly  well  developed  cell  plate  (Deb- 
ski,  '97)  which  extends  almost  entirely  across  the  cell,  presenting 
very  exceptional  conditions  among  the  thallophytes.  This  pecu- 
liarity is  in  keeping  with  other  characters  of  the  spindle,  which 
begins  its  development  outside  of  the  nuclear  membrane  and, 
lacking  centrosomes,  resembles  the  nuclear  figures  of  higher 
plants.  It  is  possible  that  nuclear  studies  upon  Chara  through- 
out ontogeny  might  show  a  variation  that  would  be  very  signifi- 
cant for  the  evolutionary  problems  concerned  with  the  structure 
of  protoplasm. 

Fairchild  ('97)  reports  a  cell  plate  for  Basidiobolus  when  the 
beak  cells  are  cut  off  from  the  gametes.  The  structure,  as  fig- 
ured and  described,  is  not,  however,  conspicuous.  He  points 
out  general  resemblances  between  cell  division  in  this  form  and 
in  the  Conjugales,  where,  as  Van  Wisselingh  (:  02)  described 
later  for  Spirogyra,  spindle  fibers  connect  the  daughter  nuclei 
.and  may  cooperate  towards  the  end  of  cell  division  with  a  cleav- 
age furrow  from  the  side  of  the  cell. 

The  conditions  in  the  Fucales  are  not  altogether  clear.  Both 
Strasburger  ('97a)  and  Farmer  and  Williams  ('98)  report  that 
the  central  spindle  disappears  in  Fucus  without  the  formation  of 
the  cell  plate  and  that  the  wall  is  developed  between  the  daugh- 
ter nuclei  in  a  region  of  granular  cytoplasm.  However,  in  Pel- 
vetia  some  of  the  radiating  fibrillae  from  opposite  sides  of  the 
daughter  nuclei  bend  around  these  structures  and  end  in  the  new 
wall.  It  is  not  plain  that  they  contribute  much  it  anything  to 
its  formation  in  the  way  of  substance,  but  it  would  seem  prob- 
able that  they  hold  a  directive  relation  to  the  structure  (Farmer 
and  Williams,  '98). 

The  Sphacelariaceae  seem  to  be  somewhat  similar  to  the  Fuca- 
les in  their  methods  of  cell  division.  The  beautiful  figures  of 


462  THE   AMERICAN  NATURALIST.     [VOL.  XXXVIII. 

Swingle  ('97)  for  Stypocaulon  give  details  of  the  region  of  the 
cytoplasm  that  forms  the  partition  wall  between  the  daughter 
nuclei.  There  is  a  zone  of  fine  meshed  protoplasm  between 
much  larger  vacuoles.  It  is  possible  that  some  very  long  fibrillae 
may  connect  the  daughter  nuclei  with  this  zone,  but  they  do  not 
form  a  cell  plate.  Consequently  the  wall  must  be  developed  in 
this  delicate  alveolar  layer,  which  probably  splits  along  some 
plane  of  vacuoles.  The  process  of  cleavage  is  then  really  related 
to  such  activities  of  vacuoles  as  occur  in  the  sporangium  of  the 
Mucorales  and  in  the  plasmodium.  But  the  position  of  the  alve- 
olar layer  may  be  determined  by  the  fibrillae,  since  it  is  always 
situated  nearest  to  the  smaller  of  the  two  daughter  nuclei. 

It  seems  likely  that  the  process  of  cleavage  in  the  Fucales  will 
be  found  to  be  similar  to  Stypocaulon  when  the  details  of  struc- 
ture in  the  internuclear  cytoplasm  is  known.  So  this  group,  with 
others,  is  likely  to  furnish  conditions  in  which  spindle  fibers  may 
determine  the  position  of  the  cell  wall  and  exert  a  directive  influ- 
ence upon  it  without  actually  laying  down  a  cell  plate.  As  has 
been  pointed  out,  the  splitting  of  the  cell  plate  is  probably  a 
cleavage  along  a  very  thin  flat  vacuole,  so  that  the  process  in  its 
essential  characters  is  the  same  as  cleavage  through  a  series  of 
vacuoles.  Thus  cleavage  by  tlie  cell  plate  is  possibly  an  out- 
growth from  that  phase  of  cleavage  by  constriction  in  which  the 
extensive  fusion  of  vacuoles  determines  the  planes  of  separation. 
The  important  advance  lies  in  the  new  factors,  introduced  through 
the  activities  of  fibrillae,  which  become  very  conspicuous  as  actual 
contributors  of  material  to  the  kinoplasmic  film  which  is  laid 
down  as  the  cell  plate.  This  function  of  the  fibrillae  probably 
developed  slowly  from  conditions  such  as  those  in  Stypocaulon 
and  Pelvetia,  where  their  influence  upon  the  position  of  the  cell 
wall,  if  any  at  all,  can  scarcely  be  more  than  directive. 

3.    Free  Cell  Formation. 

Whenever  a  nucleus  becomes  the  center  around  which  cyto- 
plasm is  gathered  and  separated  from  the  rest  of  the  cell  con- 
tents, so  that  the  new  cell  lies  freely  in  the  protoplasm  of  the 
old,  this  is  free  cell  formation.  Illustrations  are  presented  by 


No.  450.]  STUDIES   ON   THE   PLANT  CELL.  463 

the  spores  of  an  ascus,  the  oospore  of  the  Peronosporales,  the 
embryo  cells  of  Ephedra,  and  probably  other  gymnosperms,  and 
in  some  cases  seemed  to  be  exemplified  in  the  conditions  pre- 
sented by  the  egg  and  synergids  and  the  antipodals  of  the  embryo 
sac. 

Spore  formation  in  the  ascus  is  known  through  the  studies  of 
Harper  ('97  and  '99).  After  the  final  divisions  in  the  ascus  the 
nuclei  lie  in  the  cytoplasm,  each  with  an  aster  at  its  side  (Fig. 
8  e,  3).  A  delicate  prolongation  carries  the  aster  with  its  cen- 
trosphere  away  from  the  main  body  of  the  nucleus  (e,  i).  The 
rays  of  the  aster  now  bend  over  and  grow  around  the  nucleus, 
presenting  an  umbrella-like  figure  (e,  2).  They  finally  meet  on 
the  opposite  side,  and  thereby  cut  out  a  portion  of  the  cytoplasm 
which  is  included  in  the  spore.  The .  substance  of  the  aster 
fibers  forms  the  basis  of  a  kinoplasmic  film  which  becomes  the 
plasma  membrane  of  the  ascospore  and  develops  the  spore  wall 
externally  after  the  usual  method.  This  peculiar  activity  of  an 
aster  is  unparalleled  in  plant  or  animal  cells. 

Oogenesis  in  the  Peronosporales  has  been  described  in  some 
detail  by  several  authors,  but  the  process  has  not  generally  been 
called  free  cell  formation.  Yet  at  the  end  of  the  process  the 
oospore,  enveloped  by  periplasm,  lies  free  in  the  oogonium.  In 
the  beginning  the  ooplasm  gathers  in  the  center  of  the  oogonium 
as  a  denser  alveolar  region  around  that  peculiar  protoplasmic 
body  (generally  present)  the  ccenocentrum.  This  accumulation 
forces  the  vacuoles,  together  with  most  of  the  nuclei,  to  the 
periphery,  where  they  lie  in  a  sort  of  protoplasmic  froth  next 
the  cell  wall  and  constitute  the  periplasm.  The  spore  wall  de- 
velops at  the  boundary  of  the  ooplasm,  so  that  it  lies  close  to  the 
large  vacuoles  (Fig.  8/)  in  the  periplasm.  There  must  be  an 
accumulation  of  kinoplasm,  perhaps  from  the  plasma  membranes 
of  numerous  vacuoles,  to  form  a  delicate  layer  between  the  two 
regions  of  the  oogonium.  This  layer  of  kinoplasm  probably 
splits  along  the  line  of  vacuoles  between  the  ooplasm  and  peri- 
plasm, for  the  primary  walls  are  certainly  established  between 
two  plasma  membranes,  because  the  secondary  layers  are  added 
to  it  from  both  sides.  Nuclei  in  division  frequently  lie  very 
close  to  the  boundary  of  the  ooplasm,  but  there  is  no  evidence 


464  THE   AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

that  the  kinoplasmic  membrane  has  any  relation  to  these  mitotic 
figures.  That  is  to  say,  there  are  no  fibrillae  to  contribute  sub- 
stance to  the  membrane,  and  its  development  must  be  concerned 
with  vacuoles  alone.  In  this  respect  the  process  recalls  the  part 
played  by  vacuoles  in  the  plasmodium  and  in  certain  sporangia 
during  cleavage  by  constriction. 

Free  cell  formation  after  the  method  in  the  egg  of  Ephedra 
(Strasburger,  '79),  which  is  also  likely  to  be  found  among  other 
gymnosperms,  takes  place  during  the  differentiation  of  the  em- 
bryo cells.  The  cytoplasm  collects  around  each  nucleus,  forming 
a  sphere  (Fig.  8  g),  and  a  wall  is  developed  on  the  outside  of 
this  body.  Details  of  the  process  are  not  known,  and  it  is  not 
clear  whether  the  position  of  the  membrane  is  determined  by  the 
vacuoles  that  must  border  upon  this  region  or  whether  there  are 
fibers  radiating  from  the  nucleus  which  might  lay  down  a  cell 
plate  around  the  denser  protoplasm ;  but  the  evidence  favors  the 
former  possibility. 

Somewhat  similar  conditions  are  presented  in  the  egg  appa- 
ratus of  many  embryo  sacs.  In  certain  forms  (e.  g.,  the  lily  so 
well  described  by  Mottier,  '98)  the  egg  nucleus  and  synergids  are 
thickly  invested  by  radiating  fibers,  and  these,  together  with  the 
cell  plates,  may  readily  determine  the  position  of  the  plasma 
membrane  that  forms  the  cell  wall.  But  fibers  do  not  seem  to 
be  conspicuously  present  in  the  egg  apparatus  of  many  other 
embryo  sacs  (Excellent  illustrations  can  be  found  among  the 
Ranunculaceae).  In  these  cases  the  protoplasm  collects  around 
the  nuclei  as  dense  areas  bordered  by  vacuolar  cytoplasm,  and  it 
is  possible  that  the  vacuoles  by  fusing  with  one  another  cut  out 
these  respective  regions  and  thus  determine  the  plasma  mem- 
branes of  the  egg  and  synergids.  Such  processes  would  extend 
the  activities  of  vacuoles,  which  accompany  cleavage  by  constric- 
tion in  the  thallophytes,  to  the  highest  groups  of  plants. 

It  is  curious  that  with  all  of  the  work  upon  the  embryo  sac 
we  should  know  less  about  the  segmentation  of  the  protoplasm 
around  the  synergid,  antipodal,  and  segmentation  nuclei  in  this 
structure  than  in  the  sporangia  of  the  molds,  the  ascus,  or  dur- 
ing spore  formation  in  the  Myxomycetes. 

( To  be  continued]. 


No.  450.]  STUDIES   ON  THE   PLANT  CELL.  465 

LITERATURE  CITED   FOR  SECTION   II. 
ALLEN. 

:01.      On  the  origin  and  nature  of  the  middle  lamella.     Bot.  Gaz.  32,  I. 
ALLEN. 

:  03.     The  early  stages  of  spindle  formation  in  the  pollen  mother  cells  of 

Larix.     Ann.  of  Bot.  17,  281. 
BELAJEFF. 

'94.     Zur  Kenntniss  der  Karyokinese  bei  der  Pflanzen.     Flora,  79,  430. 
BLACKMAN. 

'98.      The  cytological  features  of  fertilization  and  related  phenomena  in 
Pinus  silvestris  L.     Phil.  Trans.  Roy.  Soc.  of  London,   190,  395. 
CHAMBERLAIN. 

'99.     Oogenesis  in  Pinus  laricio.     Bot.  Gaz.  27,  268. 
CHAMBERLAIN. 

:  03.     Mitosis  in  Pellia.     Bot.  Gaz.  26,  29. 
COKER. 

:  03.     On  the  Gametophytes  and  Embryo  of  Taxodium.     Bot.  Gaz.  36,  i 

and  1 14. 
DAVIS. 

'98.     Kerntheilung  in  der  Tetrasporenmutterzelle  bei  Corallina  officinalis 

L.  var.  mediterranea.     Ber.  d.  deut.  bot.  Gesell.  16,  266. 
DAVIS. 

'99-     The  spore  mother-cell  of  Anthoceros.     Bot.  Gaz.  28,  89. 
DAVIS. 

:00.     The  fertilization  of  Albugo  Candida.     Bot.  Gaz.  29,  297. 
DAVIS. 

:01.     Nuclear  studies  on  Pellia.     Ann.  of  Bot.  15,  147. 
DAVIS. 

:03.     Oogenesis  in  Saprolegnia.     Bot.  Gaz.  35,  233  and  320. 
DEBSKI. 

'97.     Beobachtungen  iiber    Kerntheilung   bei   Chara  fragilis.     Jahrb.  f. 

wiss.  Bot.  30,  227. 
FAIRCHILD. 

'94.     Ein  Beitrag  zur  Kenntniss  der  Kerntheilung  bei  Valonia  utricularia. 

Ber.  d.  deut.  bot.  Gesell.  12,  331. 
FAIRCHILD. 

'97.     Ueber  Kerntheilung  und   Befruchtung  bei   Basidiobolus  ranarum 

Eidam.     Jahrb.  f.  wiss.  Bot.  30,  285. 
FARMER  AND  REEVES. 

'94.     On  the  occurrence  of  centrospheres  in  Pellia  epiphylla  Nees.     Ann. 

of  Bot.  8,  219.  , 

FARMER  AND  WILLIAMS. 

'96.     On  the  fertilization  and  segmentation  of  the  spores  in  Fucus.     Ann. 
of  Bot.  10,  479. 


466  THE  AMERICAN  NATURALIST.   [VOL.  XXXVIII. 

FARMER  AND  WILLIAMS. 

'98.     Contributions  to  our  knowledge  of  the  Fucaceae  ;  their  life  history 

and  cytology.     Phil.  Trans.  Roy.  Soc.  of  London,  190,  623. 
FERGUSON. 

:01«.     The  development  of  the  pollen  tube  and  division  of  the  generative 

nucleus  in  certain  species  of  Pinus.     Ann.  of  Bot.  15,  193. 
FERGUSON. 

:01£.     The  development  of  the  egg  and  fertilization  in  Pinus  strobus. 

Ann.  of  Bot.  15,  435. 
FULMER. 

'98.     Cell  division  in  Pine  seedlings.     Bot.  Gaz.  26,  239. 
GUIGNARD. 

'99.      Le  deVeloppement  du  pollen  et  la  reduction  chromatique  dans  le 

Naias  major.     Arch.  d.  Anat.  micro.  2,  455. 
HARPER. 

'97.     Kerntheilung  und  freie  Zellbildung  im  Ascus.      Jahrb.  f.  wiss.  Bot. 

30,  249. 
HARPER. 

'99.     Cell  division  in  sporangia  and  asci.     Ann.  of  Bot.  13,  467. 
HARPER. 

:00a.     Cell  and  nuclear  division  in  Fuligo  varians.     Bot.  Gaz.  30,  217. 
HOP. 

'98.     Histologische  Studien  an  Vegetationspunkten.     Bot.  Centb.  76,  65. 

HOFMEISTER. 

'67.      Die  Lehre  von  der  Pflanzenzelle.     Leipzig. 
IKENO. 

'98.  Untersuchungen  iiber  die  Entwickelung  der  Geschlechtsorgane  und 
dem  Vorgang  der  Befruchtung  bei  Cycas  revoluta.  Jahrb.  f .  wiss. 
Bot.  32,  557. 

JUEL. 

'97.     Die  Kerntheilung  in  den  Pollenmutterzellen  von  Hemerocallis  fulva 
und  die  bei  denselben  auftretenden  Unregelmassigkeiten.     Jahrb. 
f.  wiss.  Bot.  30,  205. 
KARSTEN. 

:OO.      Die  Auxosporenbildung  der  Gattungen    Cocconeis,  Surirella   und 

Cymatopleura.     Flora,  87,  253. 
LAUTERBORN. 

'96-     Untersuchungen  iiber  Bau,  Kerntheilung  und  Bewegung  der  Diato- 

meen.     Leipzig. 
MAIRE. 

:02.     Recherches  cytologique  et  taxonomique   sur   les   Basidiomycetes. 

Bull.  d.  1.  Soc.  mycol.  d.  France,  18. 
McCoMB. 

:00-  The  development  of  the  karyokinetic  spindle  in  vegetative  cells  of 
higher  plants.  Bull.  Tor.  Bot.  Club,  27,  451. 


CH 

UNIVERB.TY 


No.  450.]  STUDIES   ON   THE   PLANT  CELL.  467 

MlVAKE. 

:01-     The  fertilization  of  Pythium  de  Baryanum.     Ann.  of  Bot.  15,  653. 

MlYAKE. 

:03rt.     On  the  development  of  the  sexual  organs  of  Picea  excelsa.     Ann. 

of  Bot.  17,  351. 
MOORE. 

:03.     The  mitoses  in  the  spore  mother-cell  of  Pallavicinia.     Bot.  Gaz. 
36,  384- 

MOTTIER. 

'97.     Beitrage  zur  Kenntniss  der  Kerntheilung  in  den  Pollenmutterzellen 
einiger  Dikotylen  und  Monokotylen.     Jahrb.  f.  wiss.  Bot.  30,  169. 
MOTTIER. 

'98.     Ueber  das  Verhalten  der  Kerne  bei  der  Entwickelung  des  Embryo- 
sacks  und   die  Vorgange  bei  der  Befruchtung.     Jahrb.  f.  wiss. 
Bot.  31,  125. 
MOTTIER. 

:00-      Nuclear  and  cell  division   in   Dictyota  dichotoma.     Ann.  of  Bot. 

14,  163. 
MOTTIER. 

:  03.     The  behavior  of  the  chromosomes  in  the  spore  mother-cells  of  higher 
plants  and  the  homology  of  the  pollen  and  embryo-sac  mother- 
cell.     Bot.  Gaz.  35,  250. 
MURRILL. 

:00-     The  development  of  the  archegonium  and  fertilization    in  the  hem- 
lock spruce  (Tsuga  Canadensis  Carr.)     Ann.  of  Bot.  14,  583. 
NEMEC. 

'98ff.     Ueber   die  ausbildung  der  achromatische  Kerntheilungsfigur  im 
vegetativen   und  fortpflanzungs   Gewebe  der  hoheren    Pflanzen. 
Bot.  Centb.  74,  i. 
NEMEC. 
'98£.     Ueber  das  Centrosoma  der  tierischen  Zellen  und  die  homodyna- 

men  Organe  bei  den  Pflanzen.     Anat.  Anzeig.  14,  569. 
NEMEC. 

'99*.     Ueber    Kern    und  Zelltheilung   bei    Solanum    tuberosum.     Flora, 

86,  214. 
NEMEC. 

'99c.     Ueber  die  karyokinetische  Kerntheilung  in  der  Wurzelspitze  von 
Allium  cepa.     Jahrb.  f.  wiss.  Bot.  33,  313. 

OSTERHOUT. 

'97.     Ueber  die   Entstehung   der   karyokinetischen    Spindel    bei    Equi- 

setum.     Jahrb.  f.  wiss.  Bot.  30,  1 59. 
PALISA. 

:00.     Die    Entwickelungsgeschichte    der    Regenerationsknospen    welche 

an  den  Grundstiicken  isolirte  Wedel  von  Cystopteris  Arten  ent- 

stehen.     Ber.  d.  deut.  bot.  Gesell.  18,  398. 


468  THE  AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

ROSEN. 

'95.     Beitrage  zur  Kenntniss  der  Pflanzenzellen.     Cohns  Beitr.  z.  Biol.  d. 

Pflan.  7,  225. 
ROSENBERG. 

:03.     Ueber  die   Befruchtung  von   Plasmopara  alpina.     Bihang.  till.  k. 

svenska  vet-akad.  Handlingar.  28. 
ROWLEY. 

:03.     Some  points  in  the  structure  and  life   history  of  diatoms.     Jour. 

Quekett  Mic.  Club,  II,  2,  417. 
SACHS. 

'94.     Physiologische  Notizen  VIII,  Mechanomorphosen  und  Phylogenie. 
Flora  78,  215. 

SCHAFFNER. 

'98.     Karyokinesis  in  the  root  tips  of  Allium  cepa.     Bot.  Gaz.  26,  225. 
STEVENS,  F.  L. 

'99.     The  compound  oosphere  of  Albugo  Bliti.     Bot.  Gaz.  28,  149. 
STEVENS,  F.  L. 

:01#.     Gametogenesis  and  fertilization  in  Albugo.     Bot.  Gaz.  32,  77.- 
STEVENS,  F.  L. 

:02-     Studies  in  the  fertilization  of  the  Phycomycetes,  Sclerospora.     Bot. 

Gaz.  34,  420. 
STEVENS  AND  STEVENS. 

:  03.     Mitosis  of  the  primary  nucleus  in   Synchytrium   decipiens.     Bot. 

Gaz.  35,  405. 
STRASBURGER. 

'79.     Die  Angiospermen  und  die  Gymnospermen.     Jena. 
STRASBURGER. 

'80.     Zellbildung  und  Zelltheilung.     Jena. 
STRASBURGER. 

'95.     Karyokinetische  Probleme.     Jahrb.  f.  wiss.  Bot.  28,  151. 
STRASBURGER. 

'97«-     Kerntheilung  und  Befruchtung  bei    Fucus.     Jahrb.  f.  wiss.  Bot. 

3°,  35i- 
STRASBURGER. 

'98.      Die  pflanzlichen  Zellhaute.     Jahrb.  f.  wiss.  Bot.  31,  511. 
STRASBURGER. 

:00.     Ueber  Reductionstheilung,  Spindelbildung, -Centrosomen  und  Cili- 

enbildner  im  Pflanzenreich.     Hist.  Beitr.  6. 
SWINGLE,  D. 

:03.     Formation  of  the  spores  in  sporangia  of  Rhizopus  nigricans  and  of 

Phycomyces  nitens.     Bu.  Plant  Ind.  U.  S.  Dept.  Agri.  Bull.  37. 
SWINGLE,  W.  T. 

'97.     Zur  Kenntniss  der  Kern  und  Zelltheilung  bei  den  Sphacelariaceen. 
Jahrb.  f.  wiss.  Bot.  30,  297. 


No.  450.]  STUDIES   ON   THE   PLANT  CELL.  469 

TlMBERLAKE. 

:  00.     The  development  and  f unctionf  of  the"  cell  plate  in  higher  plants. 
Bot.  Gaz.  30,  73. 

TlMBERLAKE. 

:  02.      Development  and  structure  of  the  swarm  spores  of  Hydrodictyon. 

Trans,  wiss.  Acad.  of  Sci.,  Arts  and  Let.  13,  486. 
TREUB. 

'78.      Quelques  recherches  sur  la  r61e  du  noyau  dans  la  division  des  cel- 
lules vegetales.     Amsterdam. 
TROW. 

:01.     Biology  and  cytology  of  Pythium  ultimum.     Ann.  of  Bot.  15.  269. 
VAN  HOOK. 

:  00.     Notes  on  the  division  of  the  cell  and  nucleus  in  liverworts.     Bot. 

Gaz.  30,  394. 
VAN  WISSELINGH. 

:02.     Untersuchungen  iiber  Spirogyra,   IV  Beitrag.     Bot.  Zeit.  60,  115. 
WAGER. 

'94.     On  the  presence  of  centrospheres  in  fungi.     Ann. 'of  Bot.  8,  321. 
WAGER. 

'96      On  the  structure  and  reproduction  of  Cystopus  candidus  Lev.     Ann. 

of  Bot.  10,  295. 
WAGER. 

:00.     On  the  fertilization  of  Peronospora  parasitica.     Ann.  of  Bot.  14, 

263. 
WEBBER 

:01.     Spermatogenesis  and  fecundation  of   Zamia.     Bu.   of   Plant  Ind. 

U.  S.  Dept.  of  Agri.  Bull.  2. 
WILLIAMS,  CLARA  L. 

'99.     The  origin  of  the  karyokinetic  spindle  in  Passiflora  crerulea.     Proc. 

Cal.  Acad.  Sci.  Bot.  Ill,  i,  189. 
ZACHARIAS. 

'88.     Ueber  Kern  und  Zelltheilung.     Bot.  Zeit.  46,  33  and  51. 


VOL.  XXXVIII,  Nos.  451-452  JULY-AUGUST,  1904 

THE 

AMERICAN 
NATURALIST 


A   MONTHLY   JOURNAL 

DEVOTED  TO  THE  NATURAL  SCIENCES 
IN    THEIR   WIDEST   SENSE 


CONTENTS 

Page 

I.    Proceedings  of  the  American  Society  of  Zoologists 485 

H.    The  Anatomy  of  the  Coniferales  (Continued)     •     PROF.  D.  P.  PENHALLOW  523 
III-    A  List  of  Bermudian  Birds  seen  during  July  and  August,  1903. 

HAROLD  BOWDITCH  565 

IV.    Neritina  virginica  Variety  Minor    •       •       •       PROFESSOR  M.  M.  METCALF  565 

V.    Studies  of  the  Plant  Cell.— Ill        . DR.  B.  M.  DAVIS  571 

VI.    Notes  and  Literature :    Zoology,     Dodge's  General  Zoology,  Coues'  Key  to  595 
North  American  Birds,  Boulenger  on  the  Classification  of  Bony  Fishes, 

Notes  on  Recent  Fish  Literature  —  Palaeontology,   Eastman's    Transla-  605 

tion  of  Zittel,  Vol.   II  —  Botany,  a  new  Book  on  Ferns,  Porter's  Flora  608 
of  Pennsylvania,  The  Journals. 


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r 

STUDIES    ON    THE   PLANT    CELL.— III. 

BRADLEY  MOORE  DAVIS. 

SECTION  III.    HIGHLY  SPECIALIZED  PLANT  CELLS  AND  THEIR 

PECULIARITIES. 

VERY  much  of  our  knowledge  of  the  structure  and  behavior 
of  protoplasm  in  plants  has  been  derived  from  the  study  of  cer- 
tain cells  whose  organization  has  reached  an  exceptionally  ad- 
vanced degree  of  differentiation.  The  peculiarities  of  these 
cells  are  obvious  and  have  proved  of  great  interest  but  we  have 
as  yet  scarcely  made  a  beginning  in  the  study  which  must  trace 
and  relate  these  characteristics  of  the  most  complex  products  of 
cellular  evolution  in  plants  to  their  more  simple  progenitors. 

This  section  will  describe  in  some  detail  the  structure  and 
protoplasmic  activities  of  the  following  six  highly  specialized 
cells  :  .  i,  The  Zoospore  ;  2,  The  Sperm  ;  3,  The  Egg  ;  4,  The 
Spore  Mother-Cell ;  5,  The  Coenocyte ;  6,  The  Coenogamete. 

i.  The  Zoospore. 

Zoospores  are  interesting  not  only  for  their  own  peculiarities 
but  also  because  they  are  well  known  to  be  the  progenitors  of 
the  sexual  cells  or  gametes  which  become  later  differentiated 
into  the  egg  and  sperm.  Comparative  studies  upon  three  cells 
so  closely  related  and  yet  so  diverse  in  their  extremes  of  struc- 
ture are  sure  to  yield  important  results. 

The  zoospore  is  generally  an  uninucleate  cell,  colorless  in  the 
Fungi,  but  containing  a  chromatophore  or  plastids  in  all  other 
groups  of  thallophytes.  There  are  usually  two  or  four  cilia 
attached  to  the  anterior  pointed  end  which  is  free  from  coloring 
matter  and  at  this  region  one  may  expect  to  find  a  red  pigment 
spot.  Some  zoospores  are  exceptional  for  special  peculiarities, 
as  those  of  Vaucheria  which  are  multinucleate,  each  nucleus 


572  THE  AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

being  accompanied  by  a  pair  of  cilia,  or  those  of  CEdogonium 
whose  colorless  forward  end  bears  a  crown  of  numerous  cilia. 
The  zoospore  stands  among  the  higher  forms  for  a  type  of  motile 
organism  that  is  very  close  to  the  bottom  of  the  assemblage  of 
groups  and  developmental  lines  which  make  up  the  Algae.  The 
forms  most  closely  related  to  the  zoospore  are  in  the  family 
Chlamydomonadeae  of  the  Volvocales.  But  at  this  general 
low  level  of  the  plant  kingdom  there  are  several  groups  whose 
members  pass  most  of  their  .lives  in  motile  conditions  (Volvo- 
cales, Flagellates  and  Peridinales)  and  the  cells  of  all  of  these 
types  resemble  zoospores  to  a  greater  or  less  degree  in  their 
structure  and  habits,  so  that  this  condition  represents  a  wide- 
spread and  well  defined  stage  of  evolutionary  development. 
Therefore  when  zoospores  are  formed  in  the  life  history  of  some 
higher  plant  they  represent  a  return  on  the  part  of  the  organism 
for  a  short  time  to  the  structure  and  mode  of  life  of  an  ancestry 
perhaps  related  in  some  way  to  the  groups  that  still  have  the 
motile  habits  throughout  most  of  their  existence. 

For  these  reasons  close  comparisons  in  structure  between  the 
zoospore  and  motile  Algae  will  be  interesting  and  should  help  to 
explain  the  peculiarities  of  these  cells.  These  peculiarities 
chiefly  concern  the  organ  that  forms  the  cilia  (blepharoplast), 
which  becomes  very  complex  in  the  sperm,  and  the  pigment 
spot. 

Unfortunately  studies  upon  these  problems  have  been  few  and 
we  are  not  prepared  to  make  a  general  statement  of  the  condi- 
tions. The  most  recent  investigation  on  the  structure  of  the 
zoospore  is  that  of  Timberlake  (:  02),  but  Strasburger  has  written 
extensively  on  the  subject,  especially  in  the  Histologische  Bei- 
trage  ('92  and  :  oo).  The  later  paper  (:oo,  p.  177-215)  reviews 
the  entire  subject  of  cilia  formation.  Dangeard  has  presented 
an  account  of  the  Chlamydomonadeae,  '99,  and  in  :oi  described 
especially  Polytoma,  comparing  its  structure  with  that  of  the 
animal  spermatozoan. 

Polytoma  (see  Fig.  9  a)  is  a  colorless  organism  but  its  cell 
structure  and  life  history  place  it  unquestionably  among  the 
Chlamydomonadeae.  The  two  cilia  arise  from  a  small  body 
(blepharoplast)  situated  at  the  extremity  of  the  cell.  A  delicate 


Nos.  451-452.]     STUDIES   ON  THE   PLANT  CELL. 


573 


thread-like  structure,  which  Dangeard  calls  the  rhizoplast,  extends 
from  the  blepharoplast  into  the  cytoplasm  and  sometimes  ends 
at  the  side  of  the  nucleus  in  a  granule  (condyle).  The-c-ilia 
grow  out  from  the  blepharoplast.  This  apparatus  is  not  known 
to  bear  any  relation  to  centrosomes  or  to  the  kinoplasm  of 
nuclear  figures  present  at  the  time  of  spore  formation.  But  it 
should  be  noted  that  the  blepharoplast  is  situated  directly  under 
if  not  actually  in  the  outer  plasma  membrane,  which  is  kino- 
plasmic.  The  filamentous  connection  between  blepharoplast 
and  nucleus  is  probably  important,  especially  since  it  has  also 
been  found  in  zoospores  (Timberlake,  :  02,  for  Hydrodictyon)  but 
we  do  not  even  know  its  developmental  history  much  less  its 
function.  Further  study  will  be  necessary  to  make  clear  possi- 
ble relations  to  kinoplasm  around  the  nucleus  or  to  centrosomes. 
Consequently  Dangeard' s  comparison  of  Polytoma  to  the  animal 
spermatozoon  is  not  convincing  for  it  seems  to  be  established  for 
the  spermatozoon  that  portions  of  the  middle  piece  at  least  and 
the  flagellum  are  derived  from  a  true  centrosome.  Indeed 
from  the  meager  evidence  now  at  hand  the  blepharoplast  of 
Polytoma  is  as  likely  to  be  a  structure  differentiated  from  the 
plasma  membrane  as  to  have  any  relation  to  the  nucleus.  But 
detailed  studies  on  sporogenesis  may  discover  a  history  more  in 
harmony  with  that  of  Hydrodictyon. 

We  have  summarized  a  portion  of  Timberlake's  (:O2)  account 
of  sporogenesis  for  Hydrodictyon 
in  the  previous  section  under  the 
head  of  "  Cleavage  by  constric- 
tion." We  shall  consider  now 
certain  details.  Small  spherical 
bodies  are  found  at  the  poles  of 
the  spindles  during  nuclear  divi- 
sion in  the  mother-cell.  They  are 
undoubtedly  accumulations  of  kino- 
plasm and  perhaps  stand  for  centro- 
somes. However  they  have  no 
polar  radiations  nor  could  they  be 
followed  between  mitoses  when  the 
nuclei  were  in  resting  conditions. 


FIG.  9. — The  Zoospore.  a,  Polytoma;  6, 
Hydrodictyon  ;  c,  Development  in  Oedo- 
gonium.  (a,  after  Dangeard  :  01 ;  b,  Tim- 
berlake :  02  ;  c,  Strasburger'92.) 


It  is  not  probable  therefore 


574  THE  AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

that  these  structures  are  permanent  in  the  cell.  After  nuclear 
multiplication  is  ended  segmentation  proceeds  until  the  nucleate 
masses  of  protoplasm  separate  from  one  another  as  zoospores. 
Then  a  body  may  be  found  lying  in  contact  with  the  plasma 
membrane  and  bearing  a  pair  of  cilia  (Fig.  9$).  This  basal  body 
(blepharoplast)  by  its  reaction  to  stains  seems  to  be  entirely 
distinct  from  the  plasma  membrane  and  is  connected  with  the 
nucleus  by  very  delicate  threads.  There  is  a  time  just  previous 
to  the  differentiation  of  the  zoospores  when  the  nuclei  lie  very 
close  to  the  cleavage  furrow  that  finally  separates  the  adjacent 
zoospore  origins.  A  granule  may  sometimes  be  observed  close 
to  these  nuclei  and  it  is  possible  that  this  is  the  first  appear- 
ance of  the  basal  body  (blepharoplast).  If  this  should  prove 
correct  the  structure  may  have  a  direct  relation  to  the  kinoplasm 
around  the  nucleus,  a  relation  that  is  afterwards  maintained 
through  the  two  or  three  delicate  fibers  that  connect  these 
structures.  Thus  the  blepharoplast  if  not  directly  derived  from 
a  centrosome  may  at  least  have  its  origin  from  the  same  region 
of  kinoplasm.  However  these  possibilities  are  mere  speculations 
and  the  investigation  of  these  points  is  very  much  to  be  desired 
in  a  number  of  algal  and  fungal  types. 

We  are  now  brought  to  the  views  of  Strasburger  as  expressed 
in  his  writings  of  '92  and  :  oo.  His  investigations  have  been 
chiefly  on  Vaucheria,  Cladophora  and  CEdogonium.  In  all  of 
these  forms  the  cilia  come  from  a  body  (blepharoplast)  which 
he  believes  to  arise  from  the  outer  plasma  membrane  (Haut- 
schicht).  The  nucleus  lies  close  to  the  plasma  membrane  at  the 
time  when  the  blepharoplast  is  formed  and  may  determine  its 
development  there  as  a  dynamic  center,  but  the  blepharoplast  is 
not  a  centrosome  according  to  Strasburger.  It  is  of  course 
kinoplasmic  since  it  develops  from  the  plasma  membrane  and 
this  would  accord  with  its  activities  as  a  cilia  forming  organ. 
The  blepharoplast  is  extraordinarily  large  in  CEdogonium  (see 
Fig.  9  c)  and  develops  a  ring  of  numerous  cilia  on  the  exterior 
while  at  the  same  time  fibrillar  rays  grow  back  into  the  cyto- 
plasm and  probably  help  to  give  a  compact  organization  to  the 
zoospore.  This  structure  is  very  suggestive  of  the  centrosphere 
and  aster  that  cuts  out  the  ascospore  (see  Section  II,  Free  Cell 


Nos.  451-452.]     STUDIES   ON   THE  PLANT  CELL.  575 

Formation)  and  in  spite  of  Strasburger's  conclusions  that  it  is 
derived  entirely  from  the  plasma  membrane  we  are  justified  in 
asking  for  a  fuller  description  of  its  development.  There  is  the 
possibility  of  a  different  origin  wherein  the  nucleus  may  play  an 
important  part  which,  in  the  light  of  Timberlake's  studies  on 
Hydrodictyon,  suggests  that  Strasburger  may  not  have  discov- 
ered the  earliest  beginning  of  the  blepharoplast  in  CEdogonium. 
And  the  same  doubts  apply  to  Cladophora  and  Vaucheria. 

There  is  thus  considerable  divergence  in  the  views  of  the 
origin  and  nature  of  the  blepharoplast  in  zoospores,  Strasburger 
believing  that  they  are  developed  as  a  specialized  region  of  the 
plasma  membrane  with  no  relation  to  centrosomes,  and  Timber- 
lake  holding  that  the  structure  in  Hydrodictyon  is  not  a  part  of 
the  plasma  membrane  but  comes  from  the  interior  of  the  proto- 
plasm. The  problem  is  also  involved  with  conditions  in  the 
sperm,  where  there  is  likewise  a  difference  of  opinion  as  to  the 
homologies  of  the  blepharoplast  but  an  undoubted  origin  at 
least  in  the  pteridophytes  and  gymnosperms  from  the  interior 
of  the  cell.  We  should  naturally  expect  the  blepharoplasts  of 
zoospores  and  sperms  to  be  homologous  and  consequently  the 
problem  is  of  great  theoretical  interest  and  will  be  taken  up 
again  in  our  discussion  of  the  sperm.  Its  solution  demands  a 
most  thorough  study  of  the  development  of  some  of  the  larger 
zoospores  as  in  CEdogonium  and  certain  species  of  the  Confer- 
valesand  Volvocales. 

The  pigment  spot  is  almost  universally  present  in  zoospores 
and  is  also  characteristic  of  the  cells  of  many  motile  organisms 
as  in  the  Volvocales  and  Flagellates  while  occasionally  found  in 
other  groups.  The  structure  has  been  called  an  eye  spot  from 
its  fancied  resemblance  to  the  simple  eyes  of  certain  Crustacea 
(Cyclops,  etc.)  but  this  term  is  unsatisfactory  since  it  is  not 
established  that  the  pigment  spot  is  primarily  a  receptive  organ 
for  light  or  warmth  ;  but  even  should  it  prove  to  be  thus  sensi- 
tive (which  is  very  probable)  thereby  orienting  the  cell  with 
respect  to  the  direction  of  incoming  rays,  that  is  not  a  function 
comparable  to  sight. 

The  coloring  matter  of  the  pigment  spot  is  held  as  a  single 
globule  or  as -a  collection  of  numerous  small  granules  in  meshes 


5  7  6  THE  AMERICA N  NA  TURALIST.  [VOL.  XXXVIII. 

of  the  protoplasm.  It  is  frequently  associated  with  a  plastid. 
The  pigment  may  be  readily  broken  down  and  dissolved  out  by 
such  reagents  as  alcohol  and  ether.  In  chemical  composition  it 
is  very  close  to  haematochrome  and  thus  may  be  related  to 
chlorophyll  or  a  derivative  of  that  substance.  The  cytoplasm 
around  the  pigment  spot  is  undifferentiated  and  when  the  color- 
ing matter  is  removed  it  is  very  difficult  and  sometimes  impos- 
sible to  find  the  situation  of  the  structure.  Consequently  the 
pigment  spot  can  hardly  be  considered  a  protoplasmic  organ 
since  it  is  merely  an  accumulation  of  coloring  matter  at  some 
point  in  the  cell.  Strasburger  (:oo,  p.  193)  states  that  the 
pigment  spot  of  certain  zoospores  (Cladophora,  etc.)  is  formed 
in  the  plasma  membrane  but  this  is  not  true  of  many  other 
motile  cells  (Flagellata)  and  there  is  no  doubt  that  in  some  cells 
(e.  g.  the  gametes  of  Cutleria)  the  pigment  spot  is  a  portion  of 
a  plastid.  The  literature  upon  the  structure  and  function  of 
pigment  spots  is  reviewed  by  Zimmermann  (Beitrage  z.  hot. 
Centralb.  Bd.  4,  p.  159,  1894)  and  since  then  Wager  ('99)  has 
presented  a  detailed  study  of  Euglena. 

2.  The  Sperm. 

The  sperm  is  unquestionably  derived  from  the  zoospore 
through  primitive  types  of  gametes  which  were  identical  with 
zoospores  in  all  essentials  of  morphology.  I  have  described  the 
origin  and  evolution  of  sexual  cells  of  plants  in  two  recent 
papers  (Popular  Science  Monthly,  Nov.  1901,  p.  66  and  Feb. 
1902,  p.  300).  We  should  expect  the  simplest  forms  of  sperms 
to  have  the  characters  of  zoospores  and  this  is  the  fact.  The 
sperms  of  the  Algae,  as  a  rule,  have  the  same  number  of  cilia 
(usually  two)  as  their  ancestral  asexual  zoospores.  They  gener- 
ally contain  a  chromatophore,  although  sometimes  much  reduced, 
and  there  is  present  the  pigment  spot.  The  cilia  are  attached 
at  the  pointed  end  or  at  the  side,  arising  from  colorless  pro- 
toplasm that  sometimes  contains  the  pigment  spot  while  the 
chromatophore,  when  present,  and  the  nucleus  lie  at  some 
distance  from  this  region  of  the  cell.  The  sperms  of  bryophytes 
and  pteridophytes  are  much  attenuated  in  form  and  lack  the 


Nos.  451-452.]     STUDIES   ON   THE   PLANT  CELL.  577 

pigment  spot  and  chromatophore.  Those  of  the  bryophytes  and 
the  Lycopodinese  are  biciliate  while  other  pteridophytes  have 
multiceliate  sperms  the  cilia  being  distributed  on  a  band 
(blepharoplast)  which  lies  along  one  side  of  the  spiral  structure. 
A  large  portion  of  the  spiral  in  these  sperms  is  composed  of 
nuclear  substance  and  much  of  the  remaining  cytoplasm  with 
granules  and  vacuolar  inclusions  may  frequently  be  found  in  a 
vesicle  attached  to  the  larger  end  of  the  spiral. 

The  only  motile  sperm  among  the  Fungi  is  that  of  Mono- 
blepharis.  The  male  cells  of  other  Fungi  are  non-motile 
bodies  (spermatia)  generally  formed  from  the  ends  of  delicate 
filaments  which  are  found  in  special  organs  called  spermagonia. 
Spermagonia  have  been  described  in  the  Uredinales,  the  lichens 
and  in  the  Laboulbeniaceae  but  their  function  is  only  clearly 
established  for  the  last  two  groups.  They  are  very  highly 
differentiated  in  the  Laboulbeniaceae  and  comprise  several  types 
of  structure.  Another  type  of  male  cell,  found  in  certain 
groups  of  the  Phycomycetes  and  Ascomycetes,  is  the  ccenogamete 
(to  be  described  presently)  which  is  however  not  the  homologue 
of  the  sperm  but  of  the  mother-cell  or  antheridium  that  develops 
such  structures.  Sperms  of  the  red  Algae  (Rhodophyceae)  are 
likewise  non-motile  and  they  are  invariably  formed  singly  in 
small  cells  at  the  ends  of  filaments.  These  non  motile  sperms 
of  Fungi  and  red  Algae  are  exceedingly  small  uninucleate  bodies 
without  further  complexity  of  structure  as  far  as  is  known. 

We  shall  not  attempt  to  discuss  the  earlier  literature  that 
treats  of  the  structure  and  development  of  the  plant  sperm.  In 
1894  Belajeff  published  a  German  translation  of  a  paper 
written  two  years  before  in  Russian  which  presents  the  views  of 
previous  investigators  and  to  this  the  reader  is  referred  for  such 
historical  references.  At  that  time  various  opinions  were  held 
respecting  the  organization  of  the  sperm,  some  writers  (Campbell, 
Guignard  and  others)  believing  that  it  was  chiefly  or  wholly 
nuclear  in  origin,  while  another  group  (Zacharias,  '87,  Belajeff, 
Strasburger,  '92,  etc.)  thought  that  the  cytoplasm  shared  very 
largely  in  its  structure.  Belajeff  ('94a)  from  studies  among  the 
Characeae  showed  with  especial  clearness  that  the  cytoplasm 
was  an  important  constituent  of  this  sperm  since  the  nuclear 


578  THE  AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

material  occupied  a  restricted  region  in  the  middle  of  the  spiral 
structure.  This  was  the  first  of  a  series  of  investigations  which 
have  given  especial  attention  to  cytoplasmic  activities  during 
spermatogenesis  and  placed  the  entire  subject  in  a  new  light. 

The  year  1 897  brought  forth  almost  simultaneously  three'  short 
papers  by  Webber  ('9/a,  '9/b,  '9/c)  and  Belajeff  ('97a,  '9/b, 
'9/c)  respectively.  Webber  had  studied  the  development  of  the 
motile  sperms  of  Zamia  and  Ginko,  Belajeff  certain  forms  of  the 
Filicineae  and  P^quisetineae.  These  were  of  the  nature  of  pre- 
liminary announcements  and  both  authors  published  later  more 
detailed  descriptions  and  discussions.  The  discoveries  of  motile 
sperms  in  Ginko  by  Hirase  and  of  Cycas  by  Ikeno  were 
announced  in  several  short  papers  during  the  years  1896  and 
'97  but  without  descriptions  of  their  development.  This  litera- 
ture together  with  later  papers  of  Ikeno,  Shaw,  Belajeff,  Hirase, 
and  Fujii  is  reviewed  in  Webber's  last  contribution  (:oi)  and 
also  in  Strasburger's  discussion  of  "  Cilienbildner  "  (:  oo,  p.  177) 
to  which  the  reader  is  referred  for  the  most  complete  treatments 
of  spermatogenesis  in  plants  yet  published. 

The  cycads  and  Ginko  are  the  most  favorable  subjects  known 
for  studies  in  spermatogenesis.  Detailed  accounts  of  the  cycads 
are  given  by  Ikeno  ('98b)  for  Gycas  and  by  Webber  (:oi)  for 
Zamia,  these  forms  agreeing  with  one  another  in  all  essentials. 
Two  sperms  are  developed  from  the  daughter  cells  (spermatids) 
following  the  division  of  the  so-called  body  cell  in  the  pollen 
tube.  The  process  really  begins  in  the  body  cell  with  the 
appearance  of  the  blepharoplasts.  Their  development  has  been 
followed  with  especial  attention  in  Zamia.  They  are  formed 
de  novo  in  the  cytoplasm  at  some  distance  from  the  nucleus  and 
while  the  latter  is  in  the  resting  condition.  They  appear  inde- 
pendently of  one  another,  generally  on  opposite  sides  of  the 
nucleus  but  sometimes  much  nearer  together  (Fig.  io«).  Each 
is  a  large  deeply  staining  body  with  numerous  radiations 
extending  into  the  cytoplasm.  The  blepharoplasts  then  increase 
in  size  and,  moving  farther  away  from  the  nucleus,  take  positions 
exactly  opposite  to  one  another.  The  nucleus  of  the  body  cell 
now  divides,  its  spindle  being  clearly  intranuclear  (Fig.  5  d]  and 
consequently  holding  no  visible  relation  to  the  blepharoplasts. 


Nos.  451-452.]      STUDIES   ON    THE   PLANT  CELL. 


579 


which  lie  at  a  considerable  distance  from  the  structure  (Fig.  10  b}. 
The  latter  cannot  then  be  said  to  occupy  the  position  of  centro- 
somes  in  relation  to  this  spindle.  Meanwhile  important  changes, 
which  are  best  known  for  Zamia,  take  place  in  the  blepharoplast. 
In  this  type  the  structure  forms  a  hollow  sphere  which  breaks 
up  into  segments  and  finally  into  granules  as  mitosis  proceeds. 
The  radiations  disappear  without  holding  any  apparent  relation 
to  the  spindle.  During  telophase  each  of  the  two  blepharoplasts 


FIG.  10. —  Spermatogenesis  in  Cycas.  a,  Body  cell  in  pollen  tube  with  two  blepharoplasts  ;  s, 
stalk  cell;  /,  prothallial  cell;  b,  anaphase  of  mitosis  in  the  body  cell  the  spindle  lying 
between  the  two  blepharoplasts  which  have  begun  to  form  cilia ;  c,  Blepharoplast  elongat- 
ing, in  contact  with  a  process  from  the  nucleus;  d,  end  of  blepharoplast  attached  to  the 
nucleus  at  a  later  stage  of  development ;  e,  sperm  showing  section  of  the  flattened  spiral 
blepharoplast  with  cilia  projecting  beyond  the  cell.  (After  Ikeno,  '98.)  < 

appears  as  a  mass  of  granules  at  some  distance  from  the  daugh- 
ter nuclei  which  are  to  become  the  sperm  nuclei.  As  a  result  of 
this  division  the  spermatids  (sperm  mother-cells)  are  differen- 
tiated. At  the  close  of  the  mitosis  the  blepharoplast  enters 
upon  its  functions  of  forming  in  the  spermatid  a  cilia  bearing 
band  which  is  to  lie  as  a  spiral  around  the  sperm.  The  granules 
first  extend  as  a  delicate  deeply  stained  line  towards  the  nucleus 
and  then  in  the  opposite  direction.  The  nucleus  in  Cycas  puts 
forth  a  papilla  (Fig.  io^r)  which  meets  this  line  of  granules  and 
remains  attached  to  it  for  some  time.  The  line  thickens  into  a 


580  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

band  which  lengthens  and  finally  takes  the  form  of  a  spiral  of 
five  or  six  turns  which  becomes  more  or  less  closely  applied  to 
the  plasma  membrane  (Fig.  10  e,  blepharoplast  in  section).  The 
cilia  develop  as  protuberances  from  the  outer  surface  of  the 
band  (Fig.  loc  and  d}  and  grow  through  the  plasma  membrane 
to  the  exterior  of  the  cell.  The  nucleus  in  the  meantime  has 
increased  in  size  until  it  occupies  the  greater  part  of  the  top 
shaped  sperm  (Fig.  loe). 

The  history  of  spermatogencsis  in  Ginko  is  strikingly  parallel 
to  that  of  the  cycads.  The  chief  features  were  first  described 
by  Webber  ('97c)  and  in  greater  detail  by  Hirase  ('98).  The  two 
blepharoplasts  appear  de  novo  on  opposite  sides  of  the  nucleus 
in  the  body  cell.  They  show  the  same  high  state  of  differentia- 
tion as  those  of  the  cycads,  being  large  and  the  center  of  a 
number  of  prominent  radiations.  Ginko  however  presents  a 
peculiarity  not  reported  in  the  previous  group.  A  large  spheri- 
cal body  lies  between  each  blepharoplast  and  the  nucleus  in  an 
area  of  granular  cytoplasm.  This  structure  stains  deeply  like 
the  globules  of  nucleolar  substance  which  are  frequently  found 
in  the  cytoplasm  after  nuclear  division.  They  are  probably 
accumulations  of  a  somewhat  similar  material  at  these  points  in 
the  cell  to  be  utilized  at  later  periods  of  spermatogenesis,  since 
they  decrease  in  size  as  the  sperms  mature.  The  spindle  in  the 
body  cell  is  formed  between  the  blepharoplasts  but  its  poles  lie 
at  some  distance  from  and  are  entirely  independent  of  these 
structures.  During  this  mitosis  the  spherical  bodies  pass  to 
one  side  of  the  spindle  so  that  the  daughter  nuclei  (sperm 
nuclei)  finally  take  the  position  formerly  occupied  by  them. 
The  blepharoplast  becomes  granular  and  begins  to  lengthen  into 
a  band,  one  end  of  which  becomes  attached  to  the  nucleus  that 
puts  forth  a  small  papilla  towards  the  blepharoplast.  The  band 
elongates  and  takes  the  form  of  a  spiral  which  makes  several 
turns  around  one  end  of  the  cell  just  under  the  plasma  mem- 
brane. Cilia  then  develop  along  this  band  as  in  the  cycads. 
The  earlier  accounts,  describing  a  short  tail  on  the  sperm  were 
founded  upon  material  that  was  not  altogether  normal  and  have 
been  corrected  by  Webber  and  Fujii.  The  mature  sperms  have 
essentially  the  same  form  as  those  of  Zamia  and  Cycas. 


Nos.  451-452.]      STUDIES   ON   THE  PLANT  CELL.  581 

There  has  been  some  discussion  on  the  morphology  of  these 
motile  sperms  of  the  gymnosperms.  The  claim  has  been  made 
that  they  are  ciliated  spermatids  (sperm  mother-cells)  and  there- 
fore different  from  the  sperms  of  pteridophytes  which  are 
formed  inside  of  mother-cells  that  upon  their  escape  are  left 
behind  as  empty  cysts.  However  a  close  analysis  of  their  struc- 
ture will  show  that  the  sperms  in  both  groups  have  an  identical 
protoplasmic  organization.  There  is  a  nucleus  and  a  greater  or 
less  amount  of  cytoplasm  in  which  the  blepharoplast  lies  and  the 
entire  structure  is  surrounded  by  a  plasma  membrane.  Any 
differences  in  the  processes  of  spermatogenesis  can  only  concern 
the  greater  or  less  development  of  a  cellulose  membrane  around 
the  spermatids.  It  may  be  true  that  this  cellulose  membrane 
is  entirely  absent  in  Cycas  and  Zamia,  but  if  present  it  would 
be  merely  a  shell  like  envelope  around  the  sperm  and  cannot 
affect  its  morphological  unity  and  agreement  with  the  sperms 
of  pteridophytes.  A  comparative  study  of  the  composition  and 
formation  of  the  walls  enclosing  sperm  nuclei  in  the  sperma- 
tophytes  is  much  needed  to  carefully  distinguish  between  plasma 
membranes  and  the  cellulose  secretions  that  may  be  developed 
by  them. 

While  the  cycads  and  Ginko  have  very  much  the  largest 
sperms  known  and  are  consequently  extremely  favorable  for  an 
examination  of  spermatogenesis  nevertheless  some  surprisingly 
detailed  studies  have  been  made  among  the  Filicineae  and  Equise- 
tineae.  Following  his  preliminary  announcements  ('9/a,  '9/b, 
'9/c),  Belajeff  published  in  '98  an  account  of  spermatogenesis  in 
Gymnogramme  and  Equisetum.  These  forms  present  histories 
parallel  to  each  other  and  to  the  cycads.  Two  deeply  staining 
bodies  (blepharoplasts)  appear  on  opposite  sides  of  each  nucleus 
previous  to  the  final  mitosis  in  the  antheridium  which  differen- 
tiates the  spermatids.  Consequently  each  spermatid  receives  a 
blepharoplast  which  lies  close  beside  the  nucleus.  The  bleph- 
aroplast begins  to  elongate  and  is  followed  by  the  nucleus  so 
that  both  structures  form  two  parallel  bands  which  take  a  spiral 
form.  (Illustrated  in  Fig.  3^  of  Section  I.)  The  rest  of  the 
cytoplasm  remains  as  a  vesicle  which  comes  to  lie, at  the  larger 
end  of  the  sperm.  -  The  cilia  of  Equisetum  could  be  traced  to 


582  THE  AMERICAN  NATURALIST.    [VOL.  XXXVI I L 

definite  granules  in  the  band  as  it  develops  from  the  compact 
spherical  blepharoplast. 

There  appeared  almost  simultaneously  with  the  foregoing  con- 
tribution of  Belajeff  a  paper  by  Shaw  ('QBb)  on  Onoclea  and 
Marsilia.  Shaw  investigated  the  cell  divisions  preceding  the 
formation  of  the  spermatids  in  Marsilia  and  discovered  some 
very  interesting  conditions.  The  two  blepharoplasts  which  are 
found  in  the  mother  cell  of  the  spermatid  are  foreshadowed  by 
smaller  bodies  which  appear  at  the  poles  of  the  spindle  in  the 
two  previous  mitoses.  The  first  of  these  structures  was  called 
a  blepharoplastoid.  The  blepharoplastoid  first  appears  besides 
the  daughter  nucleus  after  the  third  mitosis  previous  to  the  dif- 
ferentiation of  the  spermatids.  There  is  therefore  one  for  each 
nucleus  of  the  grandmother  cell  of  the  spermatid.  This  bleph- 
aroplastoid divides  but  the  halves  remain  close  together  and 
the  pair  passes  to  one  side  of  the  cell.  With  the  next  mitosis 
(the  second  previous  to  the  differentiation  of  the  spermatids) 
two  new  structures  are  formed  at  the  poles  of  the  spindle  and 
from  these  the  blepharoplasts  arise.  They  accompany  each 
daughter  nucleus  after  this  mitosis  into  the  mother-cell  of  the 
spermatid.  Then  each  divides  and  the  two  blepharoplasts  pass 
to  opposite  sides  of  the  nucleus  which  prepares  for  the  final 
mitosis  of  the  series.  This  division  gives  a  daughter  nucleus  to 
each  blepharoplast  and  the  spermatid  is  thus  organized.  The 
later  history  of  the  spermatid  as  it  changes  into  the  sperm  is 
identical  with  Belajeff 's  results. 

Belajeff  ('99)  followed  Shaw's  account  of  Marsilia  with  a  study 
of  the  same  form  and  came  to  very  different  conclusions  which 
have  to  do  chiefly  with  his  belief  that  the  blepharoplast  is  a  cen- 
trosome,  a  view  that  will  presently  be  considered  in  connection 
with  the  opinions  of  Strasburger  and  others.  Belajeff  found 
centrosome  like  bodies  (blepharoplastoids  of  Shaw)  at  the  poles 
of  spindles  in  various  mitoses  preceding  the  formation  of  the 
spermatids  with  their  unquestioned  blepharoplasts.  He  is  not 
willing  to  concede  that  these  centrosome  like  structures  pass 
into  the  cytoplasm  to  disappear  there  as  Shaw  states  for  the 
blepharoplastoids.  He  also  found  the  blepharoplasts  at  the  poles 
of  the  spindles,  which  was  not  observed  by  Shaw,  and  holds  that 
they  have  a  part  in  spindle  formation. 


Nos.  451-452.]       STUDIES   ON   THE    PLANT  CELL.  583. 

We  are  now  prepared  to  take  a  general  survey  of  the  proc- 
esses of  spermatogenesis  to  harmonize  as  much  as  possible  the 
conflicting  opinions  respecting  the  homologies  of  the  blepharo- 
plast.  Strasburger  ( :  oo,  pp.  177-215)  has  critically  reviewed 
the  subject  and  his  conclusions  are  of  great  interest.  He  em- 
phasizes the  kinoplasmic  character  of  the  blepharoplast,  whether 
it  be  a  differentiated  region  of  the  plasma  membrane  (as  he 
believes  for  the  zoospores  of  Cladophora,  CEdogonium,  etc.)  or 
a  special  development  in  the  interior  of  the  cytoplasm  (pterido- 
phytes  and  gymnosperms).  Strasburger  thinks  that  all  kino- 
plasmic structures,  be  they  centrospheres,  centrosomes  or 
blepharoplasts,  hold  a  very  close  physiological  relation  to  the 
substance  of  the  nucleolus  and  that  their  appearance  and  size  is 
largely  the  result  of  nuclear  activities.  Accordingly  the  bleph- 
aroplast might  occupy  the  position  of  a  centrosome  without 
being  genetically  related  to  that  structure,  and  in  fact  centro- 
somes or  centrospheres  are  to  be  considered  more  as  products  of 
the  cells'  activities  than  as  self  perpetuating  permanent  organs. 
There  is  abundant  evidence  that  the  last  possibility  is  the  fact 
in  many  forms  both  plants  and  animals.  Since  centrosomes  are 
not  fpund  at  other  periods  of  the  life  history  of  gymnosperms 
and  pteridophytes,  Strasburger  concludes  that  the  blepharo- 
plasts cannot  be  genetically  related  (homologous)  with  such  a 
structure. 

Ikeno  and  Hirase  from  their  earliest  writings  have  considered 
the  blepharoplast  to  be  a  centrosome.  Ikeno  ('QSa)  held  that  the 
blepharoplast  corresponded  with  the  middle  piece  of  the  animal 
spermatozoon.  Hirase  ('94  and  '97)  although  noting  for  Ginko 
that  the  blepharoplasts  did  not  divide  and  took  no  part  in  spin- 
dle formation  nevertheless  called  them  attractive  spheres.  The 
conclusions  of  Shaw  ('98)  and  Belajeff  ('99)  for  the  same  type 
(Marsilia)  have  just  been  summarized  and  present  very  different 
points  of  view.  Belajeff  believes  that  the  blepharoplast  of  Mar- 
silia holds  the  same  relation  to  the  poles  of  the  spindles  as  a 
centrosome.  But  Belajeff's  conception  of  the  centrosome  ('99, 
p.  204)  is  that  of  a  morphological  and  dynamic  center  which 
may  or  may  not  be  easily  demonstrated  according  to  the  amount 
of  stainable  substance  present.  From  these  discussions  it  is 


^584  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

evident  that  final  judgment  cannot  be  passed  until  certain  ques- 
tions of  fact  are  established  by  reinvestigations.  Shaw  and 
Belajeff  cannot  both  be  wholly  correct  in  their  observations  and 
interpretations  and  much  depends  upon  the  exactness  of  future 
studies  upon  Marsilia,  other  pteridophytes,  and  in  the  bryo- 
phytes.  The  problems  are  also  related  to  the  processes  of 
zoospore  formation  among  the  thallophytes. 

With  respect  to  the  bryophytes  Ikeno  ( :  03)  has  recently 
published  an  account  of  spermatogenesis  in  Marchantia  poly- 
morpJia.  He  reports  for  the  mitoses  in  the  antheridium,  prelim- 
inary to  the  differentiation  of  the  sperm  mother-cells,  that  a 
centrosome  appears  at  the  side  of  each  nucleus  and  divides,  the 
two  daughter  bodies  passing  to  opposite  sides  of  the  nucleus  and 
becoming  the  poles  of  the  spindle.  He  gives  evidence  that  the 
daughter  centrosomes  sometimes  divide  again  when  at  the  poles 
of  the  spindle  in  anaphase.  The  centrosome  cannot  be  found 
at  the  side  of  the  daughter  nucleus  after  the  mitosis  is  com- 
pleted but  it  appears  when  the  nucleus  is  ready  for  the  next  divi- 
sion. Ikeno's  explanation  of  the  reappearance  of  the  centrosome 
is  unusual.  He  believes  that  the  centrosome  is  formed  within 
the  interior  of  each  nucleus  as  a  deeply  staining  body  among  the 
linin  threads.  This  body  moves  to  the  nuclear  membrane  and 
is  thrust  out  into  the  cytoplasm  through  a  protuberance  from 
the  nucleus.  It  then  lies  outside  of  the  nucleus  and  becomes 
the  functioning  centrosome,  dividing  to  form  two  centrosomes 
that  separate  to  preside  over  the  poles  of  the  spindle.  After 
the  final  mitoses  in  the  spermatogeneous  tissue  the  centrosomes 
remain  to  become  the  blepharoplasts  of  the  sperms.  Each 
blepharoplast  passes  to  the  plasma  membrane  of  its  sperm  cell 
and  develops  two  cilia.  There  is  formed  at  this  time  another 
deeply  staining  body  in  the  cytoplasm  considered  by  Ikeno  equiv- 
alent to  a  "  Nebenkorper."  The  nucleus  begins  to  elongate 
and  the  "Nebenkorper"  takes  a  position  between  it  and  the 
blepharoplast  and  in  this  manner  the  much  attenuated  sperm  is 
organized  from  the  mother-cell. 

Ikeno  considers  the  blepharoplast  of  Marchantia  to  be  actu- 
ally a  centrosome  as  shown  by  its  behavior  during  mitosis.  His 
account  therefore  in  the  main  supports  Belajeff 's  interpretation 


Nos.  451452.]      STUDIES   ON   THE   PLANT  CELL.  585 

of  the  blepharoplastoids  of  Shaw  which  as  just  described  are 
regarded  by  the  latter  author  as  centrosomes.  Both  Belajeff  and 
Ikeno  are  inclined  to  use  the  term  centrosome  with  a  looseness 
that  is  unusual  since  the  first  accounts  of  this  structure  gave  to 
it  a  place  in  the  cell  which  is  not  strictly  followed  in  these 
authors'  descriptions  of  spermatogenesis.  Ikeno's  account  of 
the  intranuclear  origin  of  the  centrosome  is  extraordinary. 
Intranuclear  centrosomes  have  been  reported  in  several  animal 
forms  but  they  do  not  leave  the  nucleus  in  the  manner  described 
by  Ikeno. 

On  the  whole  the  writer  is  more  in  sympathy  with  the  views 
of  Webber  (:oi,pp.  70  to  81),  Strasburger  and  Shaw  than 
those  of  the  other  authors.  Assuming  that  the  observations 
upon  the  cycads  and  Ginko  are  correct,  Webber  is  certainly 
justified  in  emphasizing  the  striking  fact  that  the  blepharoplasts 
are  completely  independent  of  the  spindle  in  the  body  cell  and 
that  they  are  formed  de  novo  at  a  distance  from  its  nucleus. 
These  are  peculiarities  which,  if  established  generally  through- 
out spermatogenesis  in  plants,  will  remove  the  processes  entirely 
from  the  activities  of  centrosomes  in  certain  thallophytes  (e.  g. 
Stypocaulon,  Dictyota)  and  in  many  animal  cells.  It  is  certainly 
to  be  expected  that  a  centrosome  when  present  will  always  hold 
an  intimate  relation  to  spindle  formation  during  mitosis.  It  need 
not  be  a  permanent  organ  in  cell  genesis  and  an  ever  increasing 
number  of  investigations  indicate  that  it  frequently  is  not. 
Therefore  many  authors  hold  that  the  centrosome  is  rather  the 
morphological  expression  of  a  dynamic  center  than  a  protoplas- 
mic structure  with  an  individuality  comparable  to  the  organs  of 
a  cell.  But  these  universal  characteristics  of  centrosomes  are 
apparently  not  present  in  the  blepharoplasts  of  the  gymnosperms 
nor,  according  to  Shaw,  in  the  pteridophytes  (Marsilia).  But 
then  the  observations  of  Belajeff  and  Ikeno  are  not  in  accord 
with  those  of  Shaw  and  it  is  possible  that  studies  in  zoospore 
formation  and  gametogenesis  among  the  thallophytes  may  pre- 
sent the  subject  in  new  lights. 

For  as  shown  in  our  discussion  of  the  zoospore  it  is  not  clear 
whether  the  blepharoplasts  in  those  cells  are  always  derived 
in  the  same  manner.  We  have  Strasburger's  view  that  the 


586  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

structures  are  thickenings  of  the  outer  plasma  membrane 
(hautschicht)  and  opposed  to  this  Timberlake's  account  for  Hydro- 
dictyon  in  which  the  blepharoplast  is  considered  as  a  structure 
independent  of  the  plasma  membrane  although  lying  in  contact 
with  it.  It  must  be  apparent  that  the  results  of  Timberlake 
are  in  essential  agreement  with  the  events  of  spermatogenesis 
in  the  pteridophytes  and  gymnosperms  while  those  of  Stras- 
burger  introduce  new  elements  in  giving  to  the  plasma  mem- 
brane the  functions  of  forming  a  blepharoplast.  The  process  of 
spore  formation  in  the  ascus  must  also  be  considered  in  this  con- 
nection for  in  that  sporangium  a  centrosphere  associated  with 
each  nucleus  develops  numerous  fibrillse  that  resemble  so  much 
a  cluster  of  cilia  as  to  suggest  at  once  a  blepharoplast-like  struc- 
ture, but  this  centrosphere  of  course  is  an  important  factor  in 
spindle  formation  during  the  mitoses  in  the  ascus.  Indeed  we 
may  well  ask  for  further  studies  in  spermatogenesis  and  zoospore 
formation  before  we  can  expect  a  solution  of  the  problem  of  the 
blepharoplast. 

Comparisons  have  been  made  between  the  sperms  of  animals 
and  plants,  and  some  authors  (e.  g.  Wilson  :  oo,  p.  175,  Belajeff 
'9/c)  consider  the  two  cells  in  essential  agreement  as  to  structure 
and  development.  However  these  views  rest  on  the  assumption 
that  the  blepharoplast  is  truly  the  homologue  of  a  centrosome. 
It  seems  to  be  established  that  the  locomotor  apparatus  of  the 
animal  spermatozoon  is  derived  chiefly  from  one  or  more  centro- 
somes,  generally  with  the  co-operation  of  archoplasm  (idiozome, 
Nebenkern)  present  in  some  form  near  the  nucleus.  It  is  true 
that  in  plants  the  locomotor  apparatus  is  derived  from  kinoplasm 
which  as  we  pointed  out  in  Sections  I  and  II  corresponds  closely 
to  the  archoplasm  of  Boveri,  but  this  is  very  far  from  implying 
that  structures  formed  by  the  archoplasm  and  kinoplasm  respec- 
tively need  be  homologous.  Indeed  both  archoplasm  and  kino- 
plasm are  distinguished  by  their  physiological  activities  rather 
than  by  their  morphological  manifestations  which  are  too  various 
to  allow  of  close  genetic  relationships.  Therefore  it  seems  far 
from  established  that  spermatogenesis  in  plants  is  along  the 
same  lines  as  in  animals,  especially  since  the  weight  of  evidence 
at  present  indicates  that  the  blepharoplast  is  not  a  centrosome. 


Nos.  451-452.]     STUDIES   ON  THE    PLANT  CELL.  587 

There  are  numerous  problems  connected  with  the  physiology 
of  the  sperm  that  bear  directly  upon  its  protoplasmic  structure. 
Some  of  these  will  be  treated  in  Section  IV  in  connectiofTwith 
processes  of  fertilization.  But  at  this  time  it  is  well  to  call 
attention  to  the  intimate  association  that  sometimes  exists 
between  the  nucleus  and  blepharoplast.  These  structures  come 
into  actual  contact  in  Cycas  and  Ginko  through  a  process  put 
forth  from  the  nucleus.  It  should  also  be  remembered  that 
Timberlake  and  Dangeard  found  the  blepharoplasts  in  the 
zoospores  of  Hydrodictyon  and  in  the  cells  of  Polytoma  con- 
nected with  the  nucleus  by  one  or  two  fibers.  The  nuclear  beak 
that  bears  the  aster  in  the  ascus  suggests  a  similar  relationship. 
These  conditions  indicate  that  the  activities  of  locomotion  may 
depend  vitally  upon  the  nucleus. 

3.  The    Egg. 

The  subject  of  fertilization  is  reserved  for  the  next  section 
(Section  IV)  of  this  series  and  the  present  account  will  deal 
only  with  the  structure  of  the  unfertilized  egg.  As  the  sperm 
is  derived  from  a  motile  gamete  identical  with  the  zoospore,  so 
the  egg  has  had  a  similar  origin.  We  have  traced  the  steps  in 
this  evolutionary  process  among  the  algae  in  a  former  paper 
(Popular  Science  Monthly,  Feb.  1903,  p.  300).  The  first  indi- 
cation of  a  differentiation  in  the  sex  of  primitive  gametes  is  one 
of  size.  The  male  gametes  tend  to  become  smaller  while  the 
female  contains  a  greatly  increased  amount  of  cytoplasm.  One 
of  the  important  factors  determining  this  differentiation  is  the 
number  of  nuclear  divisions  which  take  place  in  the  cells  that 
produce  respectively  eggs  or  sperms.  There  are  generally  a 
great  many  more  mitoses  in  antheridia  than  in  oogonia  and  con- 
sequently a  given  amount  of  protoplasm  must  be  very  much 
divided  to  provide  each  nucleus  with  its  quota  of  cytoplasm. 

The  tendency  of  oogenesis  on  the  contrary  is  to  conserve  the 
protoplasm  for  relatively  few  nuclei,  provided  for  several  eggs  or 
for  a  single  nucleus  in  a  solitary  egg,  with  the  result  that  the 
egg  cell  is  generally  richly  supplied  with  protoplasm.  Such  proc- 
esses result  in  large  cells  with  a  prominent  chromatophore  or 


588  THE  AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

numerous  plastids  and  not  infrequently  a  considerable  amount 
of  food  material.  The  primitive  female  gametes  were  provided 
with  cilia  like  the  male,  but  with  their  increase  in  size  came  a 
sluggishness  of  movement  which  resulted  in  much  shorter  peri- 
ods of  motility  on  the  part  of  these  sexual  cells.  There  are 
some  algae  (Ectocarpus  siliculosus,  Cutleria,  Aphanochaete) 
whose  motile  female  gametes  come  to  rest  shortly  after  their 
escape  from  the  oogonia  and  are  fertilized  as  quiescent  cells  by 
the  active  sperms.  These  female  gametes  at  the  time  of  fertili- 
zation behave  physiologically  like  eggs  although  their  develop- 
ment shows  a  morphology  identical  with  the  sperm.  When 
such  female  gametes  dispense  with  cilia  entirely  they  become 
eggs. 

The  absence  of  cilia  does  away  with  very  much  of  the  com- 
plexity which  we  have  just  described  for  sperms.  There  is  no 
trace  of  the  blepharoplast  in  the  egg  and  no  indication  of  the 
activities  associated  with  this  structure,  so  conspicuous  in  sper- 
matogenesis.  The  large  motile  female  gametes  of  such  Algae  as 
Bryopsis,  Cutleria,  Aphanochaete  and  certain  species  of  Chlamy- 
domonas  and  Ectocarpus  will  probably  show  some  interesting 
conditions  when  the  details  of  their  cell  structure  and  develop- 
ment are  known,  for  some  of  these  types  are  likely  to  throw  light 
on  the  relation  which  the  blepharoplast  bears  to  other  structures 
in  the  cell. 

The  eggs  of  all  plants  (Fungi  excepted)  are  believed  to  be 
richly  stocked  with  plastids  in  sharp  contrast  to  the  sperms  which 
are  entirely  destitute  of  these  structures  in  all  groups  above  the 
algae.  The  plastids  in  the  eggs  of  Algae  contain  the  pigments 
characteristic  of  the  respective  groups  giving  these  cells  a  very 
rich  coloration  and  sometimes  an  elaborate  internal  structure 
since  these  plastids  or  the  single  chromatbphore  generally  main- 
tain a  symmetrical  relation  to  the  nucleus.  Leucoplasts  (see 
Fig.  \\a)  have  been  found  in  the  eggs  of  angiosperms 
(Schimper,  '85)  but  detailed  studies  on  the  cytoplasm  of  such 
cells  in  spermatophytes,  pteridophytes  and  bryophytes  are 
greatly  to  be  desired  to  determine  the  history  of  plastids  dur- 
ing the  development  of  these  germ  cells  and  at  later  periods 
after  fertilization. 


Nos.  451-452.]     STUDIES   ON   THE  PLANT  CELL.  589 

The  distribution  of  the  plastids  in  the  eggs  of  Algae  may  be 
so  general  that  the  entire  cell  is  colored  as  in  Fucus,  Volvox  and 
Sphaeroplea.  Or,  the  plastids  may  be  largely  or  wholly-wkh- 
drawn  from  some  portion  of  the  egg.  It  is  usual  for  eggs 
retained  within  the  parent  cell  (oogonium)  to  present  a  colorless 
area  of  protoplasm  that  becomes  the  point  at  which  the  sperm 
fuses  with  the  egg.  Such  a  hyaline  region  is  called  the  recep- 
tive spot  and  is  generally  situated  (see  Fig.  lib]  at  the  side  of 
the  egg  nearest  the  pore  or  opening  in  the  oogonium  through 
which  the  sperms  enter.  Excellent  illustrations  are  presented 
among  the  Algae  in  Vaucheria  (Oltmanns,  '95),  CEdogonium 
(Pringsheim,  '58,  Klebahn,  '92)  and  Coleochaete  (Pringsheim, 
'60,  Oltmanns,  '98).  It  has  been  suggested  that  the  receptive 
spot  is  related  to  the  clear  ciliated  end  of  the  ancestral  motile 
gamete  and  zoospore  but  the  structures  have  not  been  critically 
compared  to  determine  the  precise  character  of  their  proto- 
plasmic structure  and  development.  The  receptive  spot  in 
some  forms  (Vaucheria,  CEdogonium,  Fig.  1 1  b")  lies  directly 
under  the  opening  that  is  formed  in  the  oogonium  and  its 
protoplasm  is  probably  concerned  with  the  fermentative  action 
that  destroys  the  wall  at  that  point. 

The  red  Algae  (Rhodophyceas)  do  not  have  eggs  although  in 
their  sexual  evolution  they  are  at  the  level  of  heterogamy.  The 
female  gamete  (carpogonium  with  its  trichogyne)  is  a  cell  homol- 
ogous with  an  oogonium  and  its  protoplasmic  contents  corre- 
spond to  an  egg,  but  the  protoplast  never  withdraws  from  the  cell 
wall  to  lie  freely  as  a  naked  mass  of  protoplasm  within  the 
structure.  But  the  general  agreement  of  the  carpogonium  and 
trichogyne  with  the  oogonium  and  its  neck  like  extension  in 
Coleochaete  seems  to  determine  without  doubt  the  homologies 
of  the  former. 

There  are  very  few  eggs  among  the  fungi  that  are  strictly 
comparable  to  those  of  the  Algae.  Monoblepharis  (Thaxter  '95a) 
however  unquestionably  furnishes  such  an  example.  But  the 
eggs  of  the  Saprolegniales  and  Peronosporales  are  probably  in 
the  author's  opinion  not  directly  derived  from  those  of  Algae. 
They  are  either  a  peculiar  form  of  sexual  cell  called  the  cceno- 
gamete  (Davis  :oo  and  103)  or  closely  related  to  this  structure 


590  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

which  will  be  given  a  separate  treatment  in  this  section.  The 
ccenogamete  is  the  homologue  of  a  multinucleate  gametangium 
but  its  evolutionary  tendencies  seem  to  be  towards  such  a 
reduction  in  the  number  of  nuclei  that  in  the  highest  expression 
of  its  sexual  differentiation  the  female  cell  contains  a  single 
nucleus  and  has  the  general  form  of  an  egg.  But  this  process 
of  sexual  evolution  is  entirely  independent  of  the  well  known 
lines  of  development  in  the  Algae  (Davis,  Popular  Science  MontJdy, 
Feb.  1903).  The  female  sexual  cell  of  the  Ascomycetes  (called 
the  ascogonium  or  archicarp)  is  probably  in  most  forms  the 
homologue  of  a  gametangium.  These  subjects  will  be  treated 
in  our  account  of  the  ccenogamete. 

The  egg  in  the  archegonium  of  bryophytes  and  pteridophytes 
is  generally  reported  to  have  a  clearer  region  on  the  side  nearest 
the  neck  and  this  is  called  th'e  receptive  spot.  It  is  reported 
by  Campbell  in  his  investigations  on  Pilularia  ('88),  Iscetes  ('91), 
Osmunda  ('92a),  Marsilia  ('92b),  and  Marattia  ('94),  by  Shaw  in 
Onoclea  ('98)  by  Thorn  in  Aspidium  and  Adiantum  ('99)  and 
by  Lyon  in  Selaginella  (:oi).  The  receptive  spot  is  generally 
believed  to  be  a  portion  of  the  egg  differentiated  to  receive  the 
sperm.  It  is  an  open  question  whether  this  area  is  morpholog- 
ically the  homologue  of  the  receptive  spot  in  the  eggs  of  algae 
and  the  clear  area  at  the  ciliated  end  of  motile  gametes  and 
zoospores.  The  problem  demands  a  detailed  study  of  the  finer 
protoplasmic  structure  to  determine  whether  or  not  it  is  kino- 
plasmic  in  character.  The  nucleus  is  generally  situated  near  the 
center  of  the  egg  and  the  portions  of  the  cell  farthest  away 
from  the  neck  of  the  archegonium  contain  coarsely  granulate 
protoplasm  which  is  evidently  trophoplasmic,  i.  e.,  much  of  its 
substance  is  of  the  nature  of  food  material  and  the  products  of 
metabolism.  The  leucoplasts  would  be  supposed  to  lie  in  this 
region  of  the  cell  but  we  know  nothing  of  their  presence  and 
behavior  in  the  egg  of  bryophytes  and  pteridophytes. 

The  eggs  of  gymnosperms  generally  speaking  present  sharp 
contrasts  to  those  of  pteridophytes.  They  are  very  large,  prob- 
ably the  largest  uninucleate  cells  in  the  plant  kingdom,  and 
consequently  very  attractive  for  cell  studies  and  some  of  the  best 
work  on  the  events  of  the  maturation  and  fertilization  of  plant 


Nos.  451-452.]     STUDIES   ON   THE  PLANT  CELL. 


591 


eggs  has  been  done  on  this  group  (to  be  treated  in  Section  IV). 
Passing  over  earlier  investigations  that  described  accurately  the 
general  structure  of  the  egg  of  gymnosperms  we  shall  consider 
the  results  of  a  number  of  comparatively  recent  papers  that 
treat  especially  the  pine,  spruce  (Picea),  hemlock  (Tsuga),  fir 
(Abies),  cycads,  Ginko,  Gnetum,  Taxodium,  etc. 

Oogenesjs  and  fertilization  in  the  pine  has  been  the  subject  of 
several  extensive  studies  the  chief  being  papers  by  Dixon  ('94), 
Blackman  ('98),  Chamberlain  ('99)  and  Ferguson  (:oib).  The 
protoplasm  of  the  egg  is  at  first  vacuolate  but  later  takes  on  a 
denser  structure  which  becomes  very  puzzling  because  of  numer- 


-/. s 


FIG.  ii.  —  The  Egg.  a,  Daphne,  showing  leucoplasts ;  b,  oedogonium,  showing 
receptive  spot;  c,  pine,  with  numerous  proteid  vacuoles ;  d,  embryo  sac  of  the 
lily,  gamete  nuclei  fusing,  remains  of  one  Synergid  (s)  shown,  (a,  after  Schim- 
per,  '85;  b,  Klebahn,  '92;  c,  Ferguson,  :oi.) 

ous  granular  inclusions  and  masses  of  amorphous  material  which 
together  with  fibers  present  a  very  complex  texture.  The 
fibers  are  sometimes  collected  in  fascicles  and  they  may  form  a 
sort  of  weft  at  the  periphery  of  the  egg  or  radiate  out  from  the 
nucleus  which  is  generally  surrounded  by  a  kinoplasmic  sheath. 
The  complexity  is  greatly  increased  as  the  egg  grows  older  by 
the  development  of  remarkable  structures  called  proteid  vacuoles 
(See  Fig.  1 1^)  which  have  been  especially  described  by  Blackman 
and  Ferguson.  The  number  of  proteid  vacuoles  is  exceedingly 
variable  in  the  egg  but  they  sometimes  fill  three  fourths  of  the 
structure.  They  are  spaces  in  the  cytoplasmic  reticulum  filled 


592  THE   AMERICAN  NATURALIST.    [VOL.  XXXVI II. 

with  granules  and  irregular  masses  of  a  proteid  nature  some  of 
which  stain  like  nucleoli.  The  proteid  vacuolee  were  considered 
nuclei  by  earlier  writers  (Hofmeister  and  Goroschankin)  and 
recently  this  view  has  been  revived  by  Arnold  (:  oob)  who 
describes  the  migration  of  large  numbers  of  nuclei  from  the  cells 
of  the  jacket  surrounding  the  egg  into  that  structure.  These 
results  have  not  been  confirmed  by  Ferguson  who  agrees  with 
the  interpretation  of  other  writers  that  the  resemblance  of  the 
proteid  vacuolesto  nuclei  is  superficial.  Miss  Ferguson  believes 
that  the  material  of  the  proteid  vacuoles  is  derived  in  part  from 
the  nucleoli  in  the  cells  of  the  jacket  and  from  those  in  the  egg. 
A  vacuole  is  reported  (Ferguson)  at  the  end  of  the  egg  nearest 
the  neck  of  the  archegonium  and  this  is  regarded  as  a  sort  of 
receptive  spot  since  the  pollen  tube  discharges  its  contents  into 
this  cavity.  The  egg  nucleus  is  very  large  and  its  contents  are 
not  arranged  with  the  regularity  generally  present  in  resting 
nuclei.  There  are  numerous  bodies  which  Chamberlain  believes 
to  be  chromatic  in  composition  that  look  very  much  like  nucleoli 
and  have  been  so  designated  by  that  writer.  But  there  is  gener- 
ally one  large  unquestioned  nucleolus  and  besides  this  many 
smaller  nucleoli  are  reported  by  Ferguson  as  held  in  the  linin 
reticulum.  Then  portions  of  the  linin  frequently  take  irregular 
forms  and  stain  heavily.  There  is  also  present  besides  the  linin, 
chromatin  and  nucleoli  much  granular  material  (metaplasm), 
especially  in  the  nuclei  of  younger  eggs,  which  probably  holds 
some  relation  to  the  chromatin  although  it  may  readily  be  dis- 
tinguished at  certain  times  from  that  substance. 

Recent  accounts  of  the  spruce  and  fir,  by  Miyake  (:  O3a  and 
:  O3b)  describe  conditions  very  much  as  in  the  pine.  The  egg  of 
the  spruce  (Picea)  is  apparently  not  so  fibrous  in  structure  but 
proteid  vacuoles  give  it  a  coarse  granular  structure.  He  finds 
no  evidence  in  support  of  Arnoldi's  (:  oob)  peculiar  views  that 
the  proteid  vacuoles  are  derived  from  nuclei  that  have  passed 
into  the  egg  from  cells  of  the  sheath.  They  are  simply  masses 
of  nutritive  material.  There  is  some  doubt  whether  the  vacuoles 
present  at  the  end  of  the  egg  really  represent  a  differentiated 
receptive  spot.  The  egg  of  the  fir  (Abies)  conforms  in  all 
essentials  to  the  structure  in  the  pine  and  spruce.  There  are 
numerous  proteid  vacuoles. 


Nos.  451-452.]    STUDIES   ON   THE   PLANT  CELL.  593 

It  is  probable  that  the  eggs  of  other  conifers  will  be  found  to 
present  much  the  same  protoplasmic  structure  and  activities  as 
those  of  the  pine.  Thus  Murrill  (:  oo)  describes  for  thehejmlock 
spruce  (Tsuga)  a  vacuolar  receptive  spot  and  figures  masses  of 
food  material  very  much  like  the  proteid  vacuoles.  The  general 
features  of  the  egg  of  Cephalotaxus  (Arnoldi,  :  ooa),  Thuja 
(Land,  :  02),  Podocarpus  (Coker,  :  02),  Taxodium  (Coker,  '03) 
have  been  recently  described  and  those  of  Abies,  Larix  and 
Taxus  are  familiar  from  older  writers  but  the  pine  remains  as 
the  type  of  conifer  in  which  the  events  of  oogenesis  are  best 
known  as  regards  the  details  of  protoplasmic  activities. 

Besides  the  pine  we  have  had  some  very  complete  investiga- 
tions on  cycads  and  Ginko  (Hirase,  '98,  Ikeno,  'gSb  and  :oi, 
Webber,  :oi).  In  some  respects  these  types  and  especially  the 
cycads  seem  to  be  the  most  favorable  of  all  the  gymnosperms 
for  the  study  of  gametes  and  the  processes  of  fertilization  (to 
be  described  in  Section  IV).  The  cytoplasm  of  the  egg  is  com- 
paratively homogeneous  in  structure  so  that  the  cell  is  relieved 
from  the  complicated  fibrous  structure  and  proteid  vacuoles 
present  in  the  pine.  Ikeno  ('98b)  finds  that  the  egg  of  Cycas 
develops  a  crater  like  depression  just  before  and  at  the  time  of 
the  fusion  of  the  sperm  thus  presenting  a  rather  highly  special- 
ized receptive  spot. 

We  know  almost  nothing  of  the  detailed  structure  of  the  egg 
in  the  Gnetales.  Ephedra  (Strasburger,  '72)  develops  arche- 
gonia  much  like  those  of  other  gymnosperms  and  we  should  not 
expect  their  eggs  to  be  materially  different  even  in  details.  But 
the  conditions  in  Tumboa  (Welwitschia)  are  peculiar  and  approach 
more  closely  those  of  angiosperms  where  the  egg  nucleus  is 
scarcely  differentiated  from  neighboring  nuclei  lying  freely  in 
the  protoplasm  at  one  end  of  the  embryo  sac.  The  eggs  of 
Tumboa  (Strasburger,  '72)  are  merely  cells  of  the  prothallus  that 
push  out  small  projections  to  meet  the  pollen  tubes.  Gnetum 
presents  a  further  simplification  or  reduction  since  the  female 
nuclei  lie  freely  in  the  protoplasm  at  one  end  of  the  embryo  sac. 
In  Gnetum  gnemon  the  lower  half  of  the  embryo  sac  is  filled 
with  a  tissue  (Lotsy  '99)  but  in  several  other  species  studied  by 
Karsten  ('92,  '93)  no  cell  walls  are  found  in  the  entire  sac  until 
after  fertilization. 


594  THE   AMERICAN  NATURALIST.    [VOL.  XXXVI II. 

The  angiosperms  present  no  especial  advance  over  Gnetum  in 
the  organization  of  the  egg  except  that  this  structure  is  generally 
reduced  to  a  single  female  nucleus  and  the  cytoplasm  immedi- 
ately around  it  (see  Fig.  u  d).  This  egg  nucleus  flanked  by 
two  companions  (synergids)  and  the  accompanying  protoplasm 
compose  the  egg  apparatus  whose  morphology  is  still  a  matter 
of  dispute.  It  is  possible  that  the  synergids  may  stand  for 
portions  of  a  reduced  archegonium,  but  the  two  nuclei  bear  such 
close  relations  to  the  egg  and  polar  nucleus  that  it  seems  very 
probable  that  they  are  homologous  with  these  structures  which 
have  clearly  defined  sexual  potentialities.  In  spite  of  the 
numerous  studies  on  embryo  sacs  in  various  groups  of  angio- 
sperms we  do  not  yet  know  precisely  how  the  cytoplasm  becomes 
gathered  around  the  egg  nucleus  and  the  synergids.  The 
spindles  that  are  formed  between  these  nuclei  in  some  types 
(e.  g.,  Lilium)  have  been  supposed  to  lay  down  walls  by  means 
of  cell  plates.  But  there  are  other  forms  in  which  the  proto- 
plasm seems  to  separate  along  planes  of  vacuoles  without  rela- 
tion to  spindle  fibers. 

( To  be  continued.) 


VOL.  XXXVIII,  No.  454.  OCTOBER,  1904 

THE 

AMERICAN 
NATURALIST 


A   MONTHLY   JOURNAL 

DEVOTED  TO  THE  NATURAL  SCIENCES 
IN    THEIR    WIDEST   SENSE 


CONTENTS 

Page 

I.    The  Anatomy  of  the  Coniferales  (concluded)          PKOF.  D.  P.  PENHAILOW      691 

II.     Studieiof  the  Plant  Cell.- IV DE.  B.  M.  DAVIS      728 

III-    The  Affinities  of  the  Ophioglossacese  and  Marsiliacese    PROF-  D.  H  CAMPBELL      761 


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STUDIES    ON    THE    PLANT    CELL.  — IV. 

BRADLEY    MOORE  DAVIS. 

SECTION  III.     HIGHLY  SPECIALIZED  PLANT  CELLS  AND 
THEIR  PECULIARITIES  (Continued}. 

4.     The  Spore  Mother-cell. 

THE  spore  mother-cell  and  its  homologues  the  pollen  mother- 
cell  and  certain  embryo-sacs  have  furnished  some  of  the  most 
interesting  subjects  for  cell  studies  in  the  plant  kingdom. 
Sporogenesis  in  all  plants  above  the  thallophytes  seems  to  be 
a  period  when  nuclear  structures  are  especially  clearly  differ- 
entiated and  when  the  mechanism  of  mitosis  reaches  the  highest 
degree  of  complexity.  These  intricate  conditions  are  only 
equalled  by  processes  in  the  development  of  the  female  game- 
tophyte  of  some  angiosperms,  and  during  endosperm  formation, 
also  in  the  events  of  spermatogenesis  and  with  the  segmentation 
of  the  egg  nucleus  of  certain  gymnosperms. 

Sporogenesis  is  one  of  the  critical  periods  in  the  life  history 
of  a  higher  plant  since  it  is  the  time  when  the  asexual  genera- 
tion (sporophyte)  passes  over  to  the  sexual  (gametophyte).  This 
provides  certain  important  features  such  as  the  reduction  phe- 
nomena concerned  with  chromosomes  and  greatly  adds  to  the 
interest  in  these  cells.  These  matters  will  receive  special  atten- 
tion in  Section  V,  but  they  must  be  borne  in  mind  to  appreciate 
fully  the  significance  of  many  events  of  spore  formation. 

The  general  history  of  the  spore  mother-cell  may  be  described 
as  follows  :  It  is  the  product  of  the  last  mitosis  in  the  repro- 
ductive tissue  called  the  archesporium.  This  mitosis  always 
presents  the  number  of  chromosomes  characteristic  of  the 
sporophyte  which  is  double  the  number  found  in  the  game- 
tophyte. Therefore  the  nucleus  that  passes  into  the  spore 
mother-cell  has  the  sporophyte  number  of  chromosomes.  Two 

725 


726  THE   AMERICAN  NATURALIST.    [VoL.  XXXVIII. 

mitoses  occur  successively  in  the  spore  mother -cell  in  all  forms. 
The  first  mitosis  presents  half  the  number  of  chromosomes 
found  in  the  last  nuclear  division  in  the  archesporium  and  is 
consequently  the  reduced  or  gametophyte  number.  The  reduc- 
tion of  the  chromosomes  then  takes  place  during  the  period  of 
rest  between  the  last  mitosis  in  the  archesporium  and  the  first 
in  the  spore  mother-cell.  There  are  two  mitoses  in  the  spore 
mother-cell.  In  some  forms  these  are  exactly  alike  and  present 
essentially  the  same  characters  as  the  usual  typical  mitoses  of 
plants.  But  among  the  spermatophytes  there  are  likely  to  be 
peculiarities  in  the  arrangement  and  distribution  of  the  chromo- 
somes. In  consequence  the  first  mitosis  may  be  heterotypic 
and  the  second  homotypic  in  contrast  to  the  normal  typical  con- 
ditions. The  description  and  explanation  of  these  characters 
will  be  reserved  for  the  groups  that  illustrate  them  the  best. 
They  have  nothing  to  do  with  qualitative  reduction  phenomena 
as  was  formerly  supposed. 

There  is  sometimes  a  well  defined  period  of  rest  after  the  first 
mitosis  with  the  formation  of  a  wall  between  the  two  daughter 
nuclei,  but  frequently  the  second  mitosis  follows  immediately 
after  the  first  so  that  the  spore  mother-cell  comes  to  contain 
four  daughter  nuclei.  Cell  walls  may  then  be  formed  between 
these  nuclei  simultaneously  so  that  the  resultant  spores  are  dis- 
posed in  a  radially  symmetrical  arrangement  that  is  termed 
tripartite.  These  cell  divisions  are  almost  universally  present  in 
the  spore  mother-cell,  the  only  exceptions  being  certain  sperma- 
tophytes whose  megaspore  mother-cells  develop  directly  into 
embryo  sacs,  the  two  mitoses  (heterotypic  and  homotypic)  being 
included  within  these  structures  and  forming  a  part  of  the  game- 
tophyte history.  Why  the  number  of  spores  should  generally 
be  four  is  unexplained.  There  does  not  seem  to  be  .any  physio- 
logical significance  in  the  number  or  other  reasons  why  it  should 
not  be  more  or  less.  Indeed  it  is  somewhat  variable  in  the 
spermatophytes  for  microspore  or  pollen  mother-cells  form  two 
and  three  pollen  grains  in  certain  types  and  five,  six  and  seven 
have  been  found  in  others,  while  much  larger  numbers  have 
been  occasionally  reported.  In  no  case  is  the  microspore 
mother-cell  known  to  develop  directly  into  a  pollen  grain,  al- 


No.  454-]  STUDIES   ON   THE   PLANT  CELL.  727 

though  the  megaspore  mother-cell  regularly  becomes  an  embryo 
sac  in  some  forms  (e.g.,  Lilium).  But  an  increasing  number  of 
observations  indicate  that  the  megaspore  mother-cell  generally 
develops  two,  three  or  four  potential  megaspores  although  nor- 
mally only  one  of  these  becomes  an  embryo  sac. 

The  interest  in  the,  protoplasmic  activities  of  sporogenesis  lie 
chiefly  in  the  elaborate  methods  of  spindle  formation  and  mech- 
anism of  mitosis,  in  the  organization  and  distribution  of  the 
chromosomes,  in  the  functions  and  activities  of  the  nucleolus, 
and  in  the  organization  of  the  cell  plate  and  development  of  the 
cell  wall.  There  is  a  very  extensive  literature  on  the  spore 
mother-cell  some  of  which,  however,  merely  treats  the  broad 
features  noted  in  studies  of  a  general  morphological  character  on 
the  development  of  sporophylls  or  floral  structures.  We  shall 
only  attempt  to  consider  the  most  important  contributions,  and 
for  convenience  will  begin  our  treatment  with  the  Hepaticas  and 
conclude  with  the  spermatophytes  where  the  conditions  are  the 
most  complex. 

The  Hepaticae  or  liverworts  furnish  some  remarkable  spore 
mother-cells,  and  are  now  the  subject  of  considerable  interest 
and  some  discussion.  They  were  first  brought  conspicuously  to 
the  attention  of  botanists  by  a  paper  of  Farmer  ('94)  on  Pal- 
lavicinia  decipiens.  Farmer  described  a  remarkable  series  of 
events  in  this  type.  The  nucleus  of  the  spore  mother-cell 
became  surrounded  before  division  by  dense  protoplasm  that 
extended  into  the  four  lobes  of  the  cell  in  the  form  of  a  four- 
rayed  star  which  he  called  a  "  quadripolar  spindle."  After  its 
development  four  chromatic  droplets  appeared  in  th,e  nucleus  to 
indicate  its  approaching  division.  These  chromatic  droplets 
became  four  chromosomes  which  by  division  were  doubled  in 
number.  The  eight  rod  shaped  chromosomes  moved  in  pairs 
towards  the  four  lobes  of  the  spore  mother-cell.  There  was  a 
further  division  of  each  chromosome,  making  sixteen  in  all,  and 
the  four  groups  of  four  each  passed  simultaneously  to  the  poles 
of  the  ''quadripolar  spindle"  which  persisted  to  the  end.  It 
should  be  noted  that  the  striking  peculiarities  of  Farmer's  account 
lie  in  the  division  of  the  four  primary  chromosomes  into  sixteen, 
and  in  their  simultaneous  distribution  through  a  "  quadripolar 


728  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

spindle  "  to  form  at  once  four  daughter  nuclei.  These  events 
are  unparalleled,  as  far  as  the  writer  is  aware,  in  the  plant  or 
animal  kingdom,  and  consequently  the  account  deserves  especial 
attention.  A  four-rayed  figure  around  the  nucleus  is  not  surpris- 
ing because  the  spore  mother-cell  of  the  Jungermanniales  is  four 
lobed,  and  its  centrally  placed  nucleus  lies  in  a  restricted  area. 
But  the  simultaneous  distribution  of  quadrupled  chromosomes 
to  form  four  daughter  nuclei  is  a  process  whose  establishment 
would  be  of  fundamental  significance.  Farmer  also  described  a 
centrosome  at  each  pole  of  the  "  quadripolar  spindle." 

Farmer  ('95«,  b,  and  c )  followed  his  paper  on  Pallavicinia  with 
studies  on  other  liverworts.  He  reported  the  "  quadripolar 
spindle"  in  the  early  stages  of  mitosis  in  several  of  the  Junger- 
manniales, but  did  not  find  the  quadrupling  and  simultaneous 
distribution  of  the  chromosomes  as  in  Pallavicinia.  The  "  quad- 
ripolar spindle  "  when  present  was  a  temporary  structure  replaced 
later  by  the  bipolar  spindles  of  two  successive  mitoses  with  a 
longer  or  shorter  interval  between.  Farmer  considers  the 
"  quadripolar  spindle  "  of  these  forms  as  transitional  between 
that  of  Pallavicinia  and  the  normal  bipolar  spindle.  The  Ric- 
ciales,  Marchantiales  and  Anthocerotales  present  two  successive 
mitoses  after  the  usual  manner  in  the  spore  mother-cell. 

The  writer  has  described  the  events  of  sporogenesis  in  Pellia 
(one  of  the  Jungermanniales)  in  a  paper  covering  the  nuclear 
activities  at  several  periods  in  its  life  history  (Davis,  :oi),  and 
confirmed  much  of  Farmer's  account  of  the  mitoses  in  this  spore 
mother-cell.  These  are  two  in  number  and  successive,  with  a 
very  well  defined  resting  period  between  the  first  and  the  second. 
There  is  a  four-rayed  figure  present  during  the  prophase  of  the 
first  mitosis,  and  this  seems  to  correspond  to  Farmer's  "  quad- 
ripolar spindle."  The  nucleus  lying  in  the  center  of  the  four 
lobed  spore  mother-cell  becomes  invested  by  a  kinoplasmic 
sheath  which  develops  -a  fibrillar  structure.  Many  of  these 
fibrillae  extend  into  the  lobes  of  the  spore  mother-cell  because 
the  nucleus  is  confined  to  a  narrow  space  in  the  constricted  cen- 
tral region  of  the  cell  and  the  lobes  offer  the  only  possible  relief 
for  the  crbwded  conditions.  However,^the  four-rayed  structure 
is  not  present  when  the  chromosomes  are  ready  for  distribution, 


No.  454-]  STUDIES   ON   THE  PLANT  CELL.  729 

but  there  is  found  instead  one  large,  broad  poled  spindle.  (See 
Fig.  5  e.)  A  cell  wall  is  formed  between  the  two  daughter 
nuclei  (Fig.  8  d]  which  divide  again  after  a  very  short  period  of 
rest,  the  two  spindles  lying  at  right  angles  to  one  another.  The 
poles  of  the  spindles  are  rather  blunt,  and  there  are  no  centro- 
somes  or  centrospheres  in  either  mitosis.  The  four-rayed  struc- 
ture of  prophase  must  be  regarded  as  preliminary  to  spindle 
formation  because  the  chromosomes  are  not  ready  for  distribu- 
tion, and  when  that  period  arrives  the  structure  has  been  re- 
placed by  the  true  spindle  of  the  first  mitosis.  These  facts  led 
me  to  question  Farmer's  account  of  mitotic  phenomena  in  Palla- 
vicinia  and  his  conception  of  the  "  quadri polar  spindle,"  and  I 
suggested  that  this  structure  might  prove  to  be  a  phenomenon  of 
prophase,  a  view  to  which  Farmer  (:oi)  has  taken  exception  in 
a  criticism  of  my  results. 

Recent  investigations  of  Moore  (:  03)  on  Pallavicinia  are  flatly 
contradictory  to  the  conclusions  of  Farmer  for  Pallavicinia 
decipiens  and  support  my  suggestions.  Moore  finds  that  there 
are  two  mitoses  in  the  spore  mother-cell  of  Pallavicinia  lyellii, 
the  second  (Fig.  12  c,  d}  following  immediately  upon  the  first 
{Fig.  12  b],  each  with  bipolar  spindles  and  without  centrosomes. 
The  chromosomes,  eight  in  number,  appear  in  the  usual  way 
with  each  mitosis  (Fig.  12  c,  d).  There  is  no  "  quadripolar 
spindle"  in  Farmer's  sense,  no  quadrupling  and  simultaneous 
distribution  of  the  chromosomes.  The  prophases  preceding  the 
first  mitosis  present  a  tetrahedral  form  as  is  shown  in  Fig.  12  a. 
This  is  accentuated  by  the  fibrillae  which  gather  at  the  points 
to  make  a  four-rayed  structure  extending  into  the  lobes  of  the 
spore  mother-cell.  This  condition  is  identical  with  similar  stages 
in  Pellia  and  in  other  leafy  liverworts,  and  is  a  feature  to  be 
expected  from  the  fact  that  the  spindle  fibers  develop  chiefly  or 
wholly  externally  to  the  nuclear  membrane  in  a  rather  crowded 
region  of  the  cell.  The  nucleus  at  this  time  is  unquestionably 
in  prophase  as  shown  by  the  undifferentiated  chromosomes  and 
because  this  stage  passes  immediately  into  a  bipolar  spindle  of 
the  normal  type  (Fig.  12  b).  It  seems  very  probable  that 
Farmer  was  mistaken  in  his  conclusions  for  Pallavicinia  decipi- 
ens, and  that  the  mitoses  in  the  spore  mother-cell  of  this  form 


730  THE   AMERICAN  NATURALIST.    [VoL.  XXXVIII. 

are  not  different  in  any  essentials  from  those  of  other  plants. 


FIG.  12. —  Spore  mother-cells  of  Hepatic.-e.  a,  b,  c,  d,  Pallavicinia  lyellii.  a,  Prophase  ;  the 
fibrillae  gathered  on  four  sides  of  the  nucleus  which  has  a  tetrahedral  form  pointing  into 
the  four  lobes  of  the  spore  mother-cell;  the  nuclear  membrane  has  not  yet  broken  down; 
similar  stages  of  prophase  were  probably  considered  by  Farmer  as  quadripolar  spindles. 
b,  metaphase  of  the  first  mitosis ;  the  spindle  in  all  respects  a  normal  bipolar  structure 
without  centrospheres.  c,  Metaphase  of  the  second  mitosis;  one  spindle  shown  in  side 
view,  the  other,  almost  perpendicular  to  the  first,  presents  the  eight  chromosomes  at  the 
nuclear  plate,  d,  anaphase  of  the  second  mitosis:  one  spindle  viewed  from  the  side,  the 
other  from  one  end  shows  the  group  of  eight  grand-daughter  chromosomes.  e,f,  g,  antho- 
ceros  laevis,  h,  i,  a  larger  species  from  Italy,  e,  prophase;  one  pole  of  spindle  developed. 
f,  just  after  metaphase  of  the  first  mitosis;  eight  chromosomes;  blunt  poled  spindle  with- 
out centrospheres.  gt  metaphase  of  second  mitosis;  very  small  spindle,  h,  cell  p.ate 
forming  in  the  spindle  between  two  nuclei,  z",  two  nuclei  at  the  side  of  their  respective 
chromatophores  and  the  cell  plate  between,  after  the  second  mitosis  ;  a  third  chromato- 
phore  shown  with  strands  of  protoplasm  connecting  it  with  other  regions  of  the  cell,  (a, 
b,  c,  d,  after  Moore,  :os  ;  h,  i,  after  Van  Hook,  :  oo.) 

The  "  quadripolar  spindle "  proves  to  be  nothing  more  than  a 
condition  of  prophase. 

Besides  Pellia  and  Pallavicinia,  which  are  the  most  thoroughly 
studied  of  the  lower  liverworts,  we  know  the  processes  of  sporo- 


No.  454-]  STUDIES   ON   THE  PLANT  CELL.  731 

genesis  in  the  highest  type,  Anthoceros  (Davis,  '99).  This  form 
is  exceedingly  attractive  for  such  investigations  because  the 
spore  mother-cells  may  be  found  in  all  conditions  upon  the  same 
sporophyte.  However,  the  small  size  of  the  nuclei  and  spindles 
is  a  disadvantage.  Just  previous  to  the  first  mitosis  the  nucleus 
becomes  surrounded  by  a  mesh  of  delicate  fibrillae  (kinoplasmic). 
Later  the  nucleus  takes  an  angular  form,  and  the  fibrillse  are 
found  conspicuously  at  the  prominent  poles  (Fig.  12  c).  The 
nuclear  membrane  breaks  down  and  the  fibers  become  arranged 
to  form  a  bipolar  spindle  (Fig.  12  /)  without  centrosomes  or 
centrospheres.  There  is  a  short  period  of  rest  after  the  first 
mitosis,  but  no  wall  is  formed  between  the  two  daughter  nuclei. 
The  small  spindles  of  the  second  mitosis  (Fig.  12  g)  are  like- 
wise bipolar.  They  lie  at  right  angles  to  one  another  and  the 
cell  plates  that  are  laid  down  determine,  in  part,  the  position  of 
the  walls  that  are  formed  between  the  four  granddaughter 
nuclei  and  which  divide  the  spore  in  a  tripartite  manner.  These 
cell  plates  are  very  small  (Fig.  12  Ji  and  i ),  but  they  have  been 
observed  in  a  favorable  species  of  Anthoceros  by  Van  Hook 
(  :  oo).  It  is  not  clear  how  these  plates  become  extended  to 
the  wall  of  the  spore  mother-cell  unless  (as  suggested  in  Sec.  II) 
their  edges  make  use  of  planes  of  vacuoles  when  the  protoplasm 
separates  to  develop  the  cleft  between  the  four  daughter  cells. 
The  poles  of  the  spindles  in  Anthoceros  are  flattened  and  entirely 
free  from  structures  that  might  be  considered  centrosomes. 

Other  interesting  events  of  sporogenesis  in  Anthoceros  are 
the  division  of  the  chromatophores  and  the  nuclear  condition 
termed  synapsis.  The  young  spore  mother-cell  contains  a  single 
large  chromatophore.  This  increases  greatly  in  size  and  becomes 
filled  with  starch  grains.  The  chromatophore  divides  succes- 
sively into  two  and  then  four  portions  which  arrange  themselves 
symmetrically  in  the  cell  with  the  nucleus  in  the  center.  The 
mitoses  then  follow  and  the  four  daughter  nuclei  are  distributed, 
one  for  each  chromatophore  in  the  cell.  This  provision  of  four 
chromatophores  long  before  the  mitoses  in  the  cell  seems  very 
remarkable  (Davis,  '99,  p.  94  and  95).  Synapsis  is  a  condition 
very  common  in  the  nucleus  of  spore  mother-cells  before  divi- 
sion. The  chromatic  material  becomes  gathered  into  a  compact 


732  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

mass  besides  the  nucleolus.  The  significance  of  synapsis  is  not 
clear,  but  the  subject  will  be  discussed  in  Section  VI.  How- 
ever, there  is  good  evidence  from  Anthoceros  that  the  phenome- 
non is  a  normal  event  and  not  an  artefact,  because  synapsis  is 
always  found  at  a  certain  period  of  sporogenesis,  and  nuclei  in 
neighboring  spore  mother-cells  a  little  older  or  younger  present 
their  chromatic  material  with  the  usual  arrangement  (Davis,  '99, 
p.  96  and  97). 

To  summarize  the  conditions  in  the  spore  mother-cells  of  the 
Hepaticae,  all  conclusions,  in  the  author's  opinion,  indicate  :  (i) 
That  the  spindles  develop  from  a  surrounding  weft  of  fibrillae 
without  the  assistance  of  centrosomes.  (2)  That  the  mitoses 
are  always  two  in  number  and  successive  with  the  same  number 
of  chromosomes  for  each  division.  (3)  That  the  cell  walls  may 
be  formed  successively  as  in  Pellia  and  some  other  of  the  Jun- 
germanniales  or  simultaneously,  to  give  tetrahedral  spores,  as  in 
Anthoceros,  types  of  the  Marchantiales  and  Ricciales,  Pallavi- 
cinia  and  some  companion  forms  in  the  Jungermanniales.  It 
will  be  interesting  to  note  the  essential  agreement  in  these 
matters  between  the  Hepaticse  and  the  higher  plants. 

Nothing  is  known  of  the  nuclear  activities  during  sporogenesis 
in  the  other  great  division  of  the  bryophytes,  the  mosses 
(Musci).  The  spore  mother-cells  in  this  group  are  always  small 
and  unattractive  for  cell  studies  but  the  Sphagnales  appear  to  be 
rather  the  most  promising  for  such  investigations,  which  are 
greatly  to  be  desired. 

The  pteridophytes  have  furnished  some  important  contribu- 
tions to  our  knowledge  of  the  spore  mother-cell.  There  is  first 
the  paper  of  Osterhout  ('97)  on  spindle  formation  in  Equisetum, 
which  was  one  of  a  group  of  three  contributions  (Mottier,  '97, 
Juel,  '97)  that  did  much  to  dispose  of  a  then  prevalent  belief 
that  the  development  of  the  spindle  in  higher  plants  was  con- 
trolled by  centrosomes.  This  investigation  was  followed  by 
a  study  of  Smith  (:  oo)  on  spindle  formation  in  Osmunda. 
Calkins  ('97)  and  W.  C.  Stevens  ('98^)  considered  especially 
the  formation  and  reduction  of  chromosomes  in  several  of  the 
ferns,  and  arrived  at  contradictory  conclusions.  Strasburger 
(:  oo,  p.  76  to  79)  has  reviewed  these  results  in  relation  to 
studies  of  his  own  on  Osmunda. 


No.  454.] 


STUDIES   ON   THE   PLANT   CELL. 


733 


Osterhout's  ('97)  account  of  spindle  formation  in  Equisetum 
is  noteworthy.  He  found  that  the  nucleus  of  the  spore  mother- 
cell  became  surrounded  by  a  web  of  delicate  fibrillse,  ^vhich, 
extending  radially  into  the  surrounding  cytoplasm  (Fig.  I3#), 
were  later  (Fig.  13^)  gathered  into  numerous  pointed  bundles 
or  cones.  After  the  dissolution  of  the  nuclear  membrane  these 


FIG.  13. —  Spore  mother-cells  of  Pteridophytes.  a,  6,  c,  Equisetum  limosum.  a,  prophase  of 
first  mitosis;  the  radially  disposed  fibrilla?  are  gathering  together  into  cones,  b,  prophase, 
older  than«;  the  nuclear  membrane  has  broken  down  and  the  fibrillae  have  entered  the 
nuclear  cavity;  the  cones  lie  in  two  groups  opposite  one  another,  c,  just  before  meta- 
phase ;  the  fibrillar  cones  are  nearer  together  and  the  chromosomes  have  gathered  to  form 
the  nuclear  plate,  d,  e,f,  g,  Osmunda  regalis.  d,  very  early  prophase  of  the  first  mito- 
sis; nucleus  in  the  spirem  stage  surrounded  by  a  granular  and  fibrillar  zone  of  kinoplasm. 
e,  prophase,  somewhat  older  than  d\  fibrillar  kinoplasm  showing  polarity,  f,  still  older; 
chromosomes  formed;  one  pole  of  spindle  developed,  g,  metaphase;  a  tri-polar  spindle. 
(a,  b,  c,  after  Osterhout,  '97;  d,  e,f,g,  Smith,  :oo.) 

cones  arranged  themselves  side  by  side  in  two  sets  to  form  the 
spindle  of  metaphase  (Fig.  13^).  The  spindle  is  then  from  the 
outset  multipolar,  and  even  though  some  of  the  cones  unite  when 
they  become  grouped  around  a  common  axis,  nevertheless  the 
poles  of  the  spindle  at  metaphase  show  their  composite  nature  in 
the  absence  of  a  common  focal  point  for  the  fibrillas.  There  are 
no  centrosomes  at  the  poles  and  no  reason  for  their  presence  at 
any  stage  in  the  process  of  spindle  formation. 

Smith's  (:  oo)  study  of  Osmunda   presents  an  important  con- 
firmation of  Osterhout's  conclusions  that  the  spindle  in  pterido- 


734  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

phytes  developed  without  centrosomes,  while  illustrating  a  proc- 
ess of  spindle  formation  along  somewhat  different  lines.  Smith 
distinguished  a  zone  of  kinoplasm  around  the  nucleus  previous 
to  spindle  formation.  This  zone  became  granular,  and  then  the 
granules  arranged  themselves  in  rows  to  form  fibrillae  (Fig.  13  d\ 
which,  however,  did  not  extend  into  the  cytoplasm  radially,  but 
lay  generally  parallel  to  one  another,  so  that  the  spindle  appeared 
bipolar  from  the  beginning  (Fig.  13  <?).  One  pole  of  the  spindle 
was  generally  formed  considerably  in  advance  of  the  other  (Fig. 
I3f)-  The  fibers  did  not  meet  at  a  common  point  but  over  a 
broad  area,  and  there  were  no  centrosomes.  There  is,  then,  nor- 
mally no  multipolar  stage  in  Osmunda,  although  tripolar  spindles 
(Fig.  13^-)  were  occasionally  found.  During  anaphase  secondary 
fibers  were  put  forth  from  the  vicinity  of  the  daughter  nuclei  and 
these  met  in  the  equatorial  region  of  the  cell.  The  spindle  of 
the  second  mitosis  was  formed  exactly  as  in  the  first.  After  this 
division  the  four  granddaughter  nuclei  lay  connected  with  one 
another  by  six  spindles  (two  primary  and  four  secondary).  Cell 
plates  were  laid  down  in  the  equatorial  regions  of  these  spindles 
so  that  the  protoplasm  became  divided  simultaneously  and  sym- 
metrically into  tetrahedral  spores. 

The  studies  of  Calkins  ('97)  and  Stevens  ('98^)  were  chiefly 
upon  the  division  and  distribution  of  the  chromosomes  in  con- 
nection with  reduction  phenomena.  Calkins  believed  that  the 
processes  of  sporogenesis  followed  the  same  course  as  the  matu- 
ration of  sexual  cells  in  animals,  with  a  transverse  division  to 
give  a  qualitative  reduction  in  Weismann's  sense.  Stevens  dis- 
agreed with  Calkins  in  several  particulars,  holding  that  the 
reduction  was  merely  quantitative.  Reduction  phenomena  in 
plants  is  now  much  better  understood  than  at  the  time  of  these 
papers  which  dealt  with  plants  much  more  difficult  to  study  than 
some  other  forms  (e.  g.,  types  of  the  Liliaceae).  We  shall  con- 
sider the  subject  in  Section  V,  but  may  state  now  that  Calkins' 
conclusions  have  not  been  sustained. 

Strasburger  (:oo)  gives  considerable  attention  to  spindle 
formation  in  his  well  known  review  and  critique  of  cytological 
literature.  He  proposes  the  following  classification  of  spindles 
in  higher  plants  which  lack  centrosomes.  Those  that  pass 


No.  454.]  STUDIES   ON    THE   PLANT  CELL.  735 

through  multipolar  stages  and  later  become  bipolar  are  called 
multipolar  polyarch  spindles.  When  the  spindle  has  a  well 
defined  axis  from  the  beginning,  as  is  generally  true  oft  he  cells 
in  vegetative  tissues  of  higher  plants,  it  is  termed  multipolar 
diarch.  Strasburger  has  shown  that  these  types,  while  easily 
separated  in  the  extremes,  grade  into  one  another  so  that  the 
classification  is  not  founded  on  distinctions  of  a  very  funda- 
mental character.  The  spindle  of  Osmunda,  for  example, 
resembles  a  multipolar  diarch,  but  its  method  of  development  is 
more  closely  related  to  that  of  other  spindles  in  spore  mother- 
cells  (multipolar  polyarchs)  than  to  those  of  vegetative  tissues. 

The  gymnosperms  offer  in  Larix  an  excellent  subject  for 
studies  on  the  formation  of  pollen,  and  this  type  has  been 
treated  in  several  important  papers,  notably  by  Belajeff  ('94^), 
Strasburger  ('95)  and  Allen  (:O3).  Belajeff  s  contribution  is 
important  as  the  first  investigation  that  considered  the  multi- 
polar  spindle  as  a  preliminary  stage  in  the  development  of  the 
bipolar  structure.  Other  authors,  at  this  time  and  previous  to 
his  publication,  had  noted  multipolar  and  tripolar  spindles 
(Strasburger  ('80)  and  ('88)  in  several  forms),  but  the  lily  had 
received  the  greatest  attention  in  this  connection  (Farmer  ('93) 
and  ('95^),  Strasburger  ('95),  Sargent  ('97)  and  Mottier  ('97)  ). 
Mottier's  investigation  presented  the  first  detailed  account  of 
spindle  formation  in  this  angiosperm  and  will  be  discussed 
presently. 

Allen's  (:  03)  paper  on  Larix  includes  one  of  the  best  discus- 
sions of  the  literature  bearing  on  the  subject  of  spindle  forma- 
tion that  has  yet  appeared.  He  finds  that  the  cytoplasm  around 
the  nucleus  just  previous  to  mitosis  comes  to  contain  a  loose  net- 
work of  fibrillae.  Some  of  the  fibers  may  be  followed  through 
the  nuclear  membrane  and  may  be  seen  attached  to  chromatin 
bodies  in  the  interior  (Fig.  14^).  Later  the  cytoplasmic  fibrillae 
become  arranged  radially  and  extend  from  the  nucleus  even  to 
the  outer  plasma  membrane  at  the  periphery  of  the  pollen 
mother-cell.  The  radiating  fibers  are  connected  with  one  another 
by  branches  which  indicate  that  the  structure  is  in  part  an 
expanded  condition  of  the  original  network,  but  the  fibers  also 
grow.  The  fibers  now  fold  over  so  that  they  tend  to  lie  parallel  to 


736 


THE   AMERICAN  NATURALIST.   [ VOL.  XXXVIII. 


the  surface  of  the  nucleus  and  thus  form  a  dense  felt  around 
the  nuclear  membrane.  Presently  the  nuclear  membrane  which 
was  before  a  definite  film  becomes  wavy  in  outline  and  often 
granular  in  appearance.  The  nucleolus  shows  signs  of  dissolu- 
tion and  there  is  a  marked  increase  in  the  number  of  intranuclear 
fibers,  which  are  chiefly  or  wholly  of  nuclear  origin.  After  the 


FIG.  14. —  Pollen  or  microspore  mother-cells  of  spermatophytes.  a,  b,  c,  Larix  europea.  a, 
prophase  of  first  mitosis ;  kinoplasmic  fi brills  forming  a  felt  around  the  nucleus,  b,  late 
prophase ;  the  nuclear  membrane  has  broken  down  and  the  interior  space  has  become  filled 
with  fibrillae  which  have  gathered  lo  form  a  multipolar  spindle,  c,  metaphase;  a  completed 
spindle  with  polar  .radiations,  d,  e,  Lilium  candidum,  d,  prophase  of  first  mitosis  ;  the 
kinoplasmic  fibrillae  have  formed  a  net  around  the  nucleus  and  are  gathered  into  several 
cones  which  would  have  become  poles  of  the  spindle,  e,  late  prophase ;  the  nuclear  mem- 
brane has  disappeared  and  the  fibril  ae  are  entering  the  nuclear  cavity  ;  several  cones  of  the 
fibrillje  constitute  the  multipolar  spindle.  f,  Agave  Americana.  Prophase  of  the  first 
mitosis  ;  the  spindle  cones  on  the  upper  side  have  pushed  through  the  special  membrane 
around  the  nucleus,  (a,  b,  c,  after  Allen,  :  03  ;  d,  e,  Mottier,  '97  ;  f,  Osterhout,  :  02.) 

disappearance  of  the  nuclear  membrane  some  of  the  peripheral 
fibers  push  outward  to  form  several  cones  of  a  multipolar  figure 
(Fig.  14  b).  The  fibers  attached  to  the  chromosomes  gather 
into  bundles  that  extend  towards  these  poles.  Finally  the  bun- 
dles of  fibers  become  more  regular  and  straighten  out  so  that 
they  come  to  lie  approximately  parallel  to  one  another,  and  thus 


No.  454.]  STUDIES   ON   THE   PLANT  CELL.  737 


the  multipolar  structure,  developing  a  distinct  axis  (Fig. 
becomes  bipolar  (multipolar  polyarch).  There  is  no  central 
body  at  the  poles  and  no  place  for  a  centrosome  in  this  develop- 
mental history. 

The  first  detailed  study  of  spindle  formation  in  Angiosperms 
was,  as  before  stated,  that  of  Mottier  ('97)  which  treated  especi- 
ally of  Lilium,  Podophyllum  and  Helleborus.  This  paper  with 
one  by  Juel  ('97)  on  Hemerocallis  and  Osterhout  ('97)  on  Equi- 
setum  effectually  disposed  of  previous  views  very  generally  held 
(Guignard,  '91,  followed  by  other  authors),  that  spindle  forma- 
tion and  mitotic  phenomena  in  higher  plants  was  involved  with 
the  activities  of  centrosomes  or  other  kinoplasmic  centers. 
Mottier  found  that  the  nucleus  in  the  pollen  mother-cell  of  the 
lily  became  invested  just  before  mitosis  with  radiating  fibers  that 
shortly  after  increased  in  quantity  to  form  a  felted  web  around 
the  structure.  Some  of  the  fibers  gathered  into  cones  (Fig. 
14  d]  which  pointed  towards  the  periphery  of  the  cell  so  that 
there  resulted,  with  the  disappearance  of  the  nuclear  membrane 
and  the  entrance  of  the  fibers  into  the  nuclear  cavity,  a  multi- 
polar  spindle  (Fig.  14  c).  The  poles  gradually  came  to  lie 
parallel  to  one  another  in  a  common  axis,  some  of  them  disap- 
pearing, so  that  the  spindle  generally  became  distinctly  bipolar 
at  metaphase  (multipolar  polyarch).  Essentially  the  same  his- 
tory was  repeated  during  the  second  mitosis  in  the  lily. 

From  this  time  on  there  have  been  a  succession  of  papers 
verifying  the  general  conclusions  of  Mottier  and  Juel  and  extend- 
ing these  results  to  many  other  forms  until  now  it  seems  to  be 
well  established  that  centrosomes  are  never  present  in  the  pollen 
mother-cell  and  that  multipolar  spindles,  developed  from  felted 
stages  and  changing  to  bipolar  spindles,  may  be  expected  in 
most  if  not  all  forms.  Guignard  ('97  and  '98)  described  multi- 
polar  spindles  in  several  types  (Nymphaea,  Nuphar,  Limoden- 
dron,  etc.),  and  while  he  believed  that  these  poles  were  occupied 
by  granules  that  sometimes  fused  to  form  typical  centrosomes, 
nevertheless  he  admitted  that  the  multipolar  spindle  might  be 
formed  independently  of  centrosomes. 

The  most  important  papers  on  spindle  formation  in  Angio- 
sperms  following  those  of  Mottier  ('97  and  '98)  'and  Juel  ('97), 


738  THE   AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

have  been  Lawson  ('98)  on  Cobea,  W.  C.  Stevens  ('98^)  on 
Asclepias,  Atkinson  ('99)  on  Arisaema  and  Trillium,  Duggar 
('99)  on  Bignonia,  Wiegand  ('99)  on  Convallaria  and  Potamoge- 
ton,  Gregoire  ('99)  on  Lilium  and  Fritillaria,  Guignard  ('99)  on 
Naias,  Williams  ('99)  on  Passiflora,  Duggar  (:  oo)  on  Symplo- 
carpus  and  Peltandra,  Lawson  (:  oo)  on  Gladiolus,  Byxbee  (:  oo) 
on  Lavatera,  Andrews  (:  01)  on  Magnolia  and  Liriodendron, 
Schniewind-Thies  (:oi)  on  Galtonia  and  Osterhout  (:  02)  on 
Agave. 

Of  the  papers  listed  above  several  demand  especial  attention 
for  the  completeness  of  the  studies  on  the  early  stages  of  spindle 
formation  in  the  pollen  mother-cell.  Lawson  ('98  and  :oo) 
found  that  the  nuclei  of  Cobea  and  Gladiolus  previous  to  mitosis 
were  surrounded  by  a  zone  of  granular  kinoplasm  which  he 
named  perikaryoplasm.  This  zone  developed  a  felted  envelope 
of  fibrillse  from  which  projections  extended  to  form  the  cones  of 
a  multipolar  figure.  The  cones  by  fusing  in  two  groups  devel- 
oped the  bipolar  spindles.  The  spindle  fibers  of  Gladiolus  are 
formed  entirely  from  the  perikaryoplasm,  the  nucleolus  and  linin 
apparently  taking  no  part  in  the  development  of  the  spindle. 
The  nucleolus  remains  intact  until  after  the  dissolution  of  the 
nuclear  membrane  when  the  spindle  is  practically  completely 
organized.  Miss  Williams  ('99)  found  for  Passiflora  that  the 
nuclear  cavity  became  filled  with  a  network  developed  from  the 
linin.  The  nuclear  wall  became  also  transformed  into  a  mesh 
which  connected  the  network  from  the  linin  with  the  surround- 
ing cytoplasmic  reticulum,  thus  forming  a  continuous  system 
throughout  the  cell.  The  central  region  of  this  network, 
enclosed  by  a  granular  zone,  developed  a  multipolar  figure 
whose  poles  finally  fused  to  form  a  bipolar  spindle.  The  con- 
trast between  this  type  of  spindle  in  which  so  much  of  the 
fibrous  structure  is  derived  from  the  linin  and  that  of  Gladiolus 
just  described  is  very  marked.  A  granular  region  outside  of 
the  fibrous  network  around  the  nucleus  is  much  more  conspic- 
uous in  Lavatera,  described  by  Byxbee  (:  oo),  than1  in  Passiflora. 
It  forms  in  Lavatera  a  dense  zone  that  suggests  a  gathering  of 
nutritive  material  (deutoplasm).  The  fibrillae  are  developed  as  a 
felt  around  the  nuclear  membrane  and  enter  the  nuclear  cavity 


No.  454.]  STUDIES   ON   THE  PLANT  CELL.  739 

with  the  breaking  down  of  this  structure.  The  fibers  gather 
into  projecting  cones  presenting  a  multipolar  structure,  and  two 
of  these,  becoming  more  prominent,  absorb  the  others  and~thus 
form  a  bipolar  spindle. 

One  of  the  most  recent  studies  on  spindle  formation  is  that  of 
Osterhout  (:  02)  on  Agave.  This  investigation  is  of  especial 
interest  for  the  extensive  experimentation  in  the  technique  of 
fixation.  The  author  proposes  a  new  terminology  for  the  stages 
of  mitosis  that  need  not  be  presented  here.  Agave  offers  a 
striking  peculiarity  in'  the  presence  of  a  special  membrane 
around  the  early  stages  of  the  spindle.  The  fibrillae  form  inside 
of  this  membrane  and  finally  push  through  it  radially  into  the 
exterior  cytoplasm  where  they  gather  into  cones  (Fig.  14  /). 
The  cones  separate  into  two  opposite  groups  with  a  general 
parallel  arrangement  of  the  fibers  and  in  this  manner  a  bipolar 
spindle  is  formed. 

It  is  becoming  possible  to  make  some  general  statements 
respecting  the  methods  of  spindle  formation  in  the  spore 
mother-cell.  Just  previous  to  prophase  it  is  almost  always 
possible  to  differentiate  a  region  of  kinoplasm  around  the 
nucleus.  This  zone  has  been  found  to  be  either  granular,  e.  g., 
Pellia,  Anthoceros  (Davis,  '99  and  :oi),  Osmunda  (Smith,  :oo), 
Cobea  and  Gladiolus  (Lawson,  '98  and  :oo),  or  it  presents  the 
appearance  of  a  fibrous  reticulum,  e.  g.,  Equisetum  (Osterhout, 
'97),  Larix  (Allen,  :  03),  Lilium  (Mottier,  '97  and  '98),  etc. 
The  latter  condition  probably  develops  from  the  former  by  the 
arrangement  of  granules  into  fibers  and  the  gradual  expansion  of 
a  very  close  network  thus  formed  into  a  coarser  structure.  The 
fibers  in  this  reticulum  sometimes  surround  the  nucleus  as  with 
a  heavy  web.  They  later  extend  radially  into  the  cytoplasm, 
partly  by  the  expansion  of  the  network  and  partly  by  their  own 
growth  and  frequently  take  a  radial  arrangement.  In  some 
instances  the  spindle  fibers  are  developed  very  largely  within 
the  nucleus  from  the  linin  (Passiflora,  Williams,  '99).  They 
then  become  gathered  into  bundles  or  groups  forming  the  cones 
which  collectively  constitute  a  multipolar  figure  that  is  often 
called  a  multipolar  spindle.  By  the  rearrangement  of  these 
cones  somewhat  parallel  to  one  another,  together  with  more  or 


740  THE   AMERICAN  NATURALIST.  [VOL.  XXXVI II. 

less  fusion,  the  multipolar  structure  becomes  a  bipolar  spindle 
(multipolar  polyarch)  generally  just  previous  to  the  period  of 
metaphase.  The  formation  of  cell  plates  and  the  disappearance 
of  the  spindle  fibers  have  been  discussed  in  Section  II  under  the 
title  "  Cleavage  by  cell  plates." 

Mention  should  be  made  of  some  irregularities  in  the  division 
and  distribution  of  the  chromosomes  that  are  conspicuous  in  cer- 
tain spore  mother-cells  and  which  have  been  the  cause  of  much 
discussion.  The  subject  has  especial  reference  to  certain  older 
views  of  the  reduction  phenomena  in  plants.  Chromosomes  split 
once  longitudinally  in  all  typical  mitoses  and  the  halves  are  drawn 
apart  in  a  symmetrical  manner  which  is  very  easily  understood. 
This  division  is  really  determined  by  the  longitudinal  fission  of 
the  spirem  thread.  But  appearances  during  the  first  nuclear 
division  in  the  spore  mother-cell  of  many  forms  have  puzzled 
investigators  for  many  years  and  have  given  rise  to  a  number 
of  interpretations.  It  seems  to  be  pretty  clearly  established 
now  that  in  these  types  there  is  a  double  longitudinal  splitting 
of  the  chromosomes  at  the  time  of  this  mitosis.  The  first  divi- 
sion takes  place  during  prophase  and  the  second  follows  closely 
after  the  first  and  is  generally  clearly  seen  at  metaphase  or  dur- 
ing anaphase.  Therefore  the  chromatic  bodies  which  appear  at 
the  nuclear  plate  during  the  first  mitosis  are  in  reality  divided  or 
about  to  be  divided  into  quarters  and  they  separate  after  this 
mitosis  as  pairs  of  granddaughter  chromosomes  instead  of  simple 
daughter  elements.  These  pairs  are  either  firmly  united  at  one 
end  into  a  V  or  irregularly  drawn  out  so  that  the  bodies  have 
very  unusual  and  sometimes  bizarre  forms.  Nuclear  figures  of 
this  irregular  appearance  were  originally  described  by  Flemming 
for  the  first  mitosis  in  the  spermatocyte  of  Salamandra  and  named 
by  him  "  heterotypic."  These  in  the  spore  mother-cell  of  plants 
are  of  similar  character  and  the  designation  "  heterotypic  "  has 
been  adopted  by  botanists  for  this  condition.  The  pairs  of  chro- 
mosomes that  enter  the  daughter  nuclei  after  the  first  mitosis 
fuse  end  to  end  to  form  a  spirem  thread  which  breaks  up  again 
during  the  second  mitosis,  without  longitudinal  fission,  into  pairs 
of  chromosomes  which  are  believed  to  be  identical  with  those 
that  entered  the  nucleus  after  the  first  mitosis.  Since  there  is 


No.  454.]  STUDIES   ON   THE   PLANT  CELL.  741 

no  longitudinal  splitting  of  the  spirem  thread  before  the  second 
division  this  mitosis  differs  from  that  of  the  "typical  "  mitoses  of 
cells  and  is  called  "homotypic  "  to  distinguish  it  on  the  one  hand 
from  the  former  and  on  the  other  from  "  heterotypic  "  divisions. 
Several  illustrations  of  heterotypic  and  homotypic  mitoses  to 
be  described  presently  are  presented  in  Fig.  15,  showing  the 
peculiar  V-shaped  pairs  of  granddaughter  chromosomes,  charac- 
teristic of  the  first  group.  It  is  important  to  note  that  whatever 
the  significance  of  this  premature  fission  of  the  chromosomes 
before  the  second  mitosis  it  is  not  of  the  nature  of  a  qualitative 
reduction  division  in  Weisman's  sense.  The  details  and  signifi- 
cance of  reduction  phenomena  will  be  considered  in  other  con- 
nections (Section  V).  The  topics  discussed  above  have  been 
recently  studied  and  reviewed  by  Mottier  (:O3). 

We  have  as  yet  said  nothing  of  the  megaspore  mother-cell  in 
Spermatophytes.  An  increasing  number  of  investigations  have 
clearly  established  the  fact  that  the  embryo-sac  in  many  forms 
is  one  of  a  group  of  two,  three  or  four  cells,  each  of  which  is  a 
potential  megaspore  because  its  nucleus  contains  the  reduced 
number  of  chromosomes.  We  are  accustomed  to  think  of  the 
well  known  conditions  in  the  lily,  where  the  megaspore  mother- 
cell  develops  directly  into  the  embryo-sac.  But  this  type  with 
some  others  (e.g.,  Fritillaria,  Tulipa,  Erythronium,  etc.)  are  the 
exceptions  and  present  a  very  highly  differentiated  condition  in 
which  the  usual  developmental  history  is  shortened  in  a  very 
interesting  manner,  which  will  be  described  presently. 

The  embryo-sac  arose  undoubtedly  as  one  of  four  megaspores 
developed  after  essentially  the  same  manner  as  microspores  or 
pollen  grains,  excepting  that  their  arrangement  was  generally  in 
a  row,  which  is  even  true  of  some  pollen  grains  (e.  g.,  Asclepias, 
Zostera).  As  stated  above,  an  increasing  number  of  investiga- 
tions have  established  the  row  of  four  potential  megaspores  in  a 
large  number  of  forms  in  various  groups.  They  may  not  always 
be  distinguished  by  the  form  of  the  group,  but  their  homologies 
are  established  by  the  mitoses  that  lead  to  their  differentiation. 
Two  mitoses  are  of  course  required  to  establish  the  group  of 
four  cells  and  both  are  identified  by  the  reduced  number  of 
chromosomes.  Some  detailed  studies  on  these  mitoses  have 


742 


THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 


established  the  fact  for  certain  forms  that  the  first  is  heterotypic 
and  the  second   homotypic,  exactly  as  in  divisions  of  the  micro- 


FIG.  15. —  Embryo  sac  or  megaspore  mother  ceil  of  spermatophytes.  a,  b,  Galtonia  candicans. 
ai,  first  mitosis  in  megaspore  mother-cell.  a2,  second  mitosis.  «3,  group  of  four  mega- 
spores.  61  and  l>2,  shortly  after  metaphase  of  the  first  mitosis  (heterotypic).  £3,  meta- 
phase  of  the  second  mitosis  (homotypic).  c,  d,  Scilla  Sibirica.  ci,  megaspore  mother- 
cell.  C2,  after  the  first  mitosis,  rj,  after  the  second  mitosis,  the  lower  cell  of  the  pair  to 
become  the  embryo  sac.  C4,  after  the  second  mitosis,  the  upper  cell  of  the  pair  to  become 
the  embryo  sac.  di,  anaphase  of  the  first  mitosis  (heterotypic).  dz,  anaphase  of  the  sec- 
ond mitosis  (homotypic).  e,  Liliiim  martagon  ;  portion  of  embryo  sac  mother-sell,  nucleus 
surrounded  by  a  felt  of  fibrillae.  /,  Lilium  candidum\  embryo  sac  mother-cell,  nucleus 
surrounded  by  radiating  fibrillffi.  g,  h,  i,  Lilium  martagon.  g,  late  prophase  of  first 
mitosis  in  embryo  sac  mother-cell,  a  multipolar  spindle,  h,  anaphase  of  first  mitosis 
(heterotypic).  i,  anaphase  of  second  mitosis  (homotypic).  (a,  b,  c,  d,  after  Schniewind- 
Thies  :  01  ;  e,f,  g,  h,  i,  Mottier  '97.) 

spore  or  pollen  mother-cells.  Schniewind-Thies  (:oi)  figures 
very  completely  the  mitoses  in  Galtonia.  The  first  mitosis  in 
the  megaspore  mother-cell  (Fig.  150)  is  heterotypic  because  the 


No.  454-3  STUDIES   ON   THE  PLANT  CELL.  743 

chromosomes  (Fig.  i$b,  i,  2)  show  clearly  the  V-shaped  forms 
characteristic  of  this  division.  The  second  mitosis  (Fig.  15  b,  3) 
is  homotypic.  The  lowest  cell  of  the  group  of  four  (Fig".  15  a, 
3)  becomes  the  embryo-sac  and  the  mitoses  that  take  place 
within  it  as  the  female  gametophyte  develops  are  all  typical. 
This  account  illustrates  a  simple  history  in  megaspore  mother- 
cell  development  and  is  considered  the  first  of  three  types  in  a 
classification  proposed  by  Schniewind-Thies  (:oi). 

The  second  type  of  development  is  one  in  which  two  mega- 
spores  are  generally  developed  from  a  mother-cell  and  one  of 
these  becomes  the  functional  embryo-sac.  Schniewind-Thies 
presents  an  excellent  illustration  of  this  type  in  Scilla.  The 
first  mitosis  in  the  megaspore  mother-cell  (Fig.  1 5  c]  is  hetero- 
typic  (Fig.  15^,  i)and  results  in  two  cells  (Fig.  I5<r).  The 
second  mitosis  in  both  cells  is  homotypic  (Fig.  15  d,  2).  Either 
the  lower  (Fig.  15  c,  3)  or  the  upper  (Fig.  15  c,  4)  of  the  pair 
may  become  the  embryo-sac.  The  embryo-sac  then  includes  the 
homotypic  or  second  mitosis  within  its  development,  making  it 
the  first  nuclear  division  of  the  gametophyte  history.  The  typi- 
cal mitoses  of  the  gametophyte  begin  with  the  second  nuclear 
division  in  the  embryo-sac.  Three  megaspores  may  be  formed 
in  such  a  group  when  the  cell  of  the  pair  that  does  not  become 
the  embryo-sac  divides  again. 

The  third  type  of  development  is  illustrated  by  several  forms, 
of  which  the  best  known  are  Lilium  (Mottier,  '98  and  :  03)  and 
Tulipa  (Schniewind-Thies  :  01).  The  lily  has  been  much  studied, 
but  Mottier  presents  the  most  detailed  account  of  spindle  for- 
mation and  the  behavior  of  the  chromosomes.  He  supports  the 
observations  of  Schniewind-Thies,  based  upon  the  tulip,  and  her 
explanation  of  this  type  of  development.  The  megaspore 
mother-cell  of  the  lily  and  tulip  develops  directly  into  the 
embryo-sac.  The  first  mitosis  in  this  cell  (Fig.  1 5  //)  is  heterc- 
typic  and  the  second  (Fig.  152')  homotypic.  These  divisions 
give  the  four-nucleate  embryo-sac  and  one  more  mitosis  presents 
the  mature  structure.  This  last  is  a  typical  mitosis,  the  only  one 
found  in  the  embryo-sac  before  the  development  of  the  endo- 
sperm and  sporophyte  embryo.  Thus  the  two  mitoses  charac- 
teristic of  the  spore  mother-cell  are  here  included  within  the 


744  THE    AMERICAN  NATURALIST.     [VOL.  XXXVIII. 

embryo-sac  and  appropriated  as  a  part  of  the  gametophyte 
history. 

We  can  see  in  these  three  types  of  embryo-sac  development 
an  evolutionary  process  of  which  the  third  stage  is  plainly 
derived  from  the  simpler  second  and  first,  and  is  consequently 
a  highly  developed  and  very  complex  condition,  far  removed 
from  primitive  gametophyte  structures  among  the  angiosperms. 
The  embryo-sacs  of  these  forms  (Lilium,  Tulipa,  Fritillaria, 
Erythronium,  etc.)  are  probably  the  most  complex  spore  mother- 
cells  that  we  know  The  studies  of  Schniewind-Thies  and 
Mottier  have  been  supported  by  other  investigations,  and  more 
especially  by  the  results  of  Ernst  (:  02)  on  Paris  quadrifolia 
and  Trillium  grandiflorum,  who  followed  the  history  of  the 
heterotypic  and  homotypic  mitoses  in  these  forms  in  detail. 
They  illustrate  the  second  type  of  embryo-sac  development  in 
the  classification  of  Schniewind-Thies. 

Spindle  formation  in  the  embryo-sac  mother-cell  has  not 
received  as  much  attention  as  in  the  pollen  mother-cell,  probably 
because  material  of  the  latter  structures  may  be  obtained  much 
more  readily  than  the  former.  There  have  been  numerous 
descriptions  and  figures  of  the  spindles  but  few  accounts  in  full 
of  their  development.  Of  the  latter  the  investigation  of 
Mottier  ('98)  on  Lilium  is  the  most  complete.  This  paper  was 
written  at  the  time  when  the  centrosome  question  was  under 
discussion  and  served,  with  other  papers  on  the  spore  mother- 
cell  (Osterhont,  '97,  Juel,  '97,  Mottier,  '97)  to  discredit  the  pres- 
ence of  these  bodies  in  this  structure.  Mottier  found  that  the 
nucleus  of  the  embryo-sac  became  invested  with  a  close  network 
of  fibrillae  (Fig.  15  e)  from  which  fibers  developed  into  the  cyto- 
plasm radiating  from  the  nucleus  in  all  directions  (Fig.  i$f). 
With  the  dissolution  of  the  nuclear  membrane  the  fibrillae 
entered  the  nuclear  cavity,  filling  it  with  masses  of  fibers  which 
gathered  into  cones  to  form  a  complicated  multipolar  spindle 
(Fig.  15^).  These  cones  later  come  together  into  two  poles, 
but  even  in  the  mature  spindle  the  fibrillae  are  frequently  in  sev- 
eral groups  at  the  poles.  Essentially  the  same  history  is  repeated 
in  the  second  mitosis.  A  large  number  of  later  papers  have 
described  and  figured  multipolar  spindles  in  embryo-sacs,  con- 


No.  454.]  STUDIES   ON   THE   PLANT  CELL.  745 

firming  the  conclusions  of  Mottier  that  these  structures  are 
developed  here  after  the  same  methods  as  in  ^  the  pollen  mother - 
cell,  from  surrounding  investments  of  fibrillae  and  without  ren- 
trosomes.  Indeed  the  embryo-sac  is  remarkable  for  the  quan- 
tity of  the  cytoplasmic  fibrillae  present  during  its  mitoses. 

In  concluding  this  account  attention  should  be  called  to 
some  forms  whose  microspore  mother-cells  were  formerly  sup- 
posed to  omit  the  mitoses  of  sporogenesis  and  develop  directly 
into  pollen  grains.  These  conditions  were  reported  in  Zostera, 
the  Cyperaceae,  and  the  Asclepiadaceae.  However,  Juel  (:  oo) 
finds  the  two  mitoses  present  in  Carex  acuta,  although  three  of 
the  nuclei  break  down  and  the  cytoplasm  is  appropriated  for  the 
fourth  to  form  a  single  pollen  grain  whose  wall  is  developed 
from  that  of  the  mother  cell.  The  history  is  very  similar  to 
the  development  of  the  megaspore  in  certain  heterosporous  pteri- 
dophytes  (e.g.,  Marsilia,  Selaginella)  and  to  the  embryo-sac, 
which  functions  while  its  companion  potential  megaspores  degen- 
erate. The  development  of  the  pollen  in  the  Asclepiadaceae  has 
been  shown  to  be  normal  in  the  nuclear  activities  by  several 
investigators  (Frye,  :  01,  Strasburger,  :  01,  and  Gagner,  :  02),  the 
tetrad  consisting  of  four  pollen  grains  in  a  row,  instead  of  the 
usual  arrangement.  In  Zostera  (Rosenberg,  :oi)  there  are  lon- 
gitudinal divisions  of  the  very  much  elongated  pollen  mother-cell 
to  give  four  extraordinary  filiform  pollen  grains. 

5.     The  Coenocyte. 

This  remarkable  type  of  cell  has  reached  an  extraordinarily 
high  state  of  development  in  certain  plants,  notably  among  the 
Siphonales  and  the  filamentous  Phycomycetes  (Mucorales,  Sap- 
rolegniales  and  Peronosporales).  Coenocytes  are  multinucleate 
cells.  The  simplest  types  are  developed  by  the  limited  division 
or  fragmentation  of  a  nucleus  accompanied  by  an  increase  in  the 
size  of  the  cell  but  without  extended  growth.  Excellent  illus- 
trations are  found  in  the  older  cells  of  the  red  algae,  the  inter- 
nodal  cells  of  the  Characeae  and  in  old  parenchyma  cells  of  many 
higher  plants. 

A  higher  type  of  ccenocyte  is  presented  when  the  multinucle- 


746  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII, 

ate  cells  show  some  definite  activity  resulting  in  extensive  growth 
or  peculiarity  of  form.  Thus  some  laticiferous  coenocytes  are 
branching  tubes  that  grow  for  considerable  distances  among  the 
cells  of  the  tissues  in  which  they  are  contained.  The  embryo- 
sac  and  the  female  gametophytes  of  Selaginella  and  Isoetes  in 
the  early  stages  of  their  development  are  interesting  coenocytes. 
Among  the  lower  algae  there  are  numbers  of  cosnocytic  forms 
(e.  g.,  Hydrodictyon,  Cladophora)  whose  cells  present  very  little 
change  with  age  except  an  increase  in  size.  Yet  some  of  these 
conditions,  especially  those  illustrated  in  the  Cladophoraceae,  are 
probably  related  to  the  higher  types  of  coenocytes. 

The  best  differentiated  coenocytes  are  found  in  the  Siphon- 
ales,  Mucorales,  Saprolegniales  and  to  a  lesser  extent  among  the 
Peronosporales  and  are  especially  well  illustrated  in  a  few  aquatic 
forms,  such  as  Monoblepharis  and  Myrioblepharis.  The  pecul- 
iarities of  these  forms  lie  in  elaborate  structures  which  result 
from  the  ability  of  the  ccenocyte  to  respond  to  several  directive 
stimuli  in  its  growth.  The  most  complicated  responses  and  con- 
sequently the  most  highly  differentiated  morphology  is  shown 
among  the  Siphonales,  where  some  very  elaborate  forms  are 
found.  In  many  types  the  plant  body  is  clearly  composed  of 
root  and  shoot  regions  and  in  the  highest  expressions  (e.  g., 
some  species  of  Caulerpa)  there  are  rhizoids,  shoots  and  leaf- 
like  structures  presenting  a  remarkable  degree  of  specialization. 
The  behavior  of  the  protoplasm  in  these  most  highly  differenti- 
ated types  of  the  Siphonales  is  known  to  us  chiefly  through 
studies  of  Noll  and  Klemm. 

There  is  a  very  conspicuous  layer  of  clear  protoplasm  next  to 
the  cell  wall  which  constitutes  an  outer  plasma  membrane  (haut- 
schicht).  This  outer  plasma  membrane  is  stationary  while  the 
granular  protoplasm  within  changes  its  position  readily  and  fre- 
quently in  different  portions  of  the  plant  streaming  in  various 
directions.  The  nuclei  are  all  situated  in  the  granular  cytoplasm 
so  that  they  must  shift  their  positions  with  its  movements.  Noll 
('87)  by  a  clever  method'  of  coloring  the  cell  wall  of  living  plants 
of  Caulerpa  was  able  to  prove  that  the  forward  growth  took 
place  by  the  protoplasm  extending  beyond  the  old  wall,  thus 
adding  new  regions  of  cellulose  to  the  old.  He  called  this. 


No.  454.]  STUDIES   ON   THE   PLANT  CELL. 

method  of  growth  a  process  of  eruption  in  contrast  to  Nageli's 
conception  of  growth  by  intussusception.  Increase  in  thickness 
comes  with  the  laying  down  of  successive  lamellae  inside  the 
older  wall  and  is  consequently  growth  by  apposition.  Caulerpa 
is  very  favorable  for  such  investigations  and  Noll's  results  greatly 
strengthen  the  theory  that  a  cellulose  wall  results  from  the 
direct  transformation  of  a  plasma  membrane  in  which  carbo- 
hydrate molecules  gradually  replace  those  of  albuminous  mate- 
rial. Accordingly  the  cellulose  wall  is  not  strictly  a  secretion 
and  its  growth  is  not  by  the  intercalation  of  new  molecules 
among  the  old  (intussusception)  in  a  non-living  membrane. 

The  wide  space  in  the  interior  of  the  filaments  of  Caulerpa 
and  some  other  members  of  the  Siphonales  is  frequently  crossed 
by  cellulose  bars  at  various  angles.  These  are  at  first  strands 
of  protoplasm  which  become  gradually  filled  with  a  carbohy- 
drate material  and  finally  solidified.  Noll  ('SSa),  while  recog- 
nizing that  these  structures  may  have  value  in  strengthening 
the  filament,  believes  that  they  are  also  the  paths  of  metabolic 
exchange  between  the  interior  regions  of  the  protoplasm  and 
the  water  outside  the  plant.  They  are  surrounded  by  the 
plasma  membrane  which  in  consequence  presents  a  much  greater 
extent  of  surface  to  the  water  permeating  the  cell  wall. 

It  is  plain  that  because  of  the  constant  movement  of  the 
granular  cytoplasm  carrying  with  it  the  nuclei  which  change 
their  position  in  the  cell,  the  outer  plasma  membrane  is  the  only 
portion  of  the  protoplasm  that  can  receive  fixed  stimuli  for  an 
extended  period.  Consequently  Noll  regards  this  membrane  as 
the  responsive  or  irritable  region  of  the  cell  that  reacts  to  the 
stimuli  which  largely  or  wholly  direct  growth.  Some  of  these 
stimuli  are  well  established.  Thus  it  is  light  which  directs  the 
formation  of  leaves  and  shoots.  The  behavior  of  Caulerpa  in 
relation  to  prominent  stimuli  (light,  darkness,  gravity,  etc.)  has 
been  studied  by  Noll  ('88£)  and  Klemm  ('93).  The  latter  author 
believes  that  the  response  is  due  to  the  presence  of  foods  or 
other  substances  at  certain  points  which  make  them  especially 
sensitive  to  the  external  stimuli.  Injuries  to  a  filament  of  the 
Siphonales  brings  about  an  immediate  flow  of  protoplasm  to  the 
wounded  part  (Klemm,'  94),  after  which  the  plasma  membrane 
is  quickly  repaired  and  new  portions  of  the  wall  laid  down. 


THE   AMERICAN  NATURALIST.    [VoL.  XXXVIII. 

Mitotic  phenomena  in  the  Siphonales  is  known  to  us  only 
through  the  investigations  of  Fairchild  ('94)  on  Valonia.  He 
found  that  nuclei  in  the  same  individual  may  divide  directly  or 
indirectly.  The  first  process  is  one  of  simple  fission,  the  latter 
takes  place  with  the  formation  of  an  intranuclear  spindle. 
Studies  in  sporogenesis  and  gametogenesis  are  very  much  to 
be  desired  in  the  Siphonales  that  we  may  understand  the 
behavior  of  the  nuclei  at  these  periods.  The  author's  recent 
studies  of  oogenesis  in  Vaucheria  (Davis,  :  04^)  have  shown  an 
interesting  process  of  nuclear  degeneration  similar  to  that  in  the 
Saprolegniales  and  Peronosporales,  and  suggests  some  very  inter- 
esting lines  of  investigation. 

The  protoplasmic  structure  in  the  hyphae  of  the  larger  fila- 
mentous Phycomycetes,  especially  the  Saprolegniales  and  Perono- 
sporales, is  undoubtedly  much  the  same  as  in  the  Siphonales. 
But  the  absence  of  chlorophyll  and  the  greater  delicacy  of  the 
filaments  makes  it  more  difficult  to  recognize  the  different 
regions  of  the  protoplasm.  There  is  an  outer  plasma  membrane 
inside  of  which  the  granular  material  slowly  moves  in  proto- 
plasmic currents  that  may  sometimes  be  observed  in  rapidly 
growing  tips.  Delicate  strands  which  are  the  paths  of  stream- 
ing currents  are  beautifully  shown  in  developing  sporangia  of 
the  molds  and  the  oogonia  of  the  Saprolegniales  and  Perono- 
sporales. The  nuclei  are  undoubtedly  carried  by  the  protoplas- 
mic movements,  sometimes  collecting  in  cnnsiderable  numbers 
in  growing  regions  of  the  filaments  which  always  contain  much 
dense  protoplasm. 

Another  type  of  coenocyte,  and  in  some  respects  the  most 
remarkable,  is  the  plasmodium  of  the  Myxomycete.  These 
structures  are  too  well  known  to  need  description  here.  We 
shall  only  refer  to  them  as  they  help  to  break  down  an  old 
theory  that  the  coenocyte  is  a  compound  structure  composed  of 
many  energids,  represented  by  the  nuclei,  which  cooperate  to 
make  up  the  whole.  The  plasmodium  and  the  protoplasmic 
mass  inside  the  cellulose  tubes  of  the  Siphonales  and  Phycomy- 
cetes agree  in  all  essentials  of  structure  and  mode  of  growth. 
The  forward  growth  of  the  plasmodium,  as  is  also  true  of  the 
Amoeba,  begins  with  the  prolongation  of  the  outer  plasma  mem- 


No.  454.]  STUDIES    OX    THE   PLANT  CELL.  749 

brane  (hautschicht,  ectoplasm)  into  a  process  (pseudopodium) 
which  advances  and  is  followed  immediately  by  an  inflow  of  the 
granular  cytoplasm.  And  the  growth  of  the  filaments  of  the 
Siphonales  and  higher  Phycomycetes  is  a  pushing  forward  of 
the  outer  plasma  membrane  followed  by  the  granular  proto- 
plasm, but  this  growth  is  slow  because  the  plasma  membrane  is 
at  all  times  under  the  restraint  of  a  cellulose  envelope. 

Mention  should  be  made  of  the  remarkable  coenocytic  zoospores 
well  known  in  Vaucheria  and  also  described  by  Thaxter  ('95^), 
for  the  Phycomycete  Myrioblepharis.  In  Vaucheria  the  entire 
contents  of  the  sporangium  becomes  transformed  into  an  im- 
mense multinucleate  zoospore,  the  cilia  being  distributed  in  pairs 
above  the  nuclei.  In  Myrioblepharis  the  contents  of  a  spor- 
angium usually  forms  four  large  multiciliate  zoospores. 

These  zoospores  of  Vaucheria  have  often  been  called  com- 
pound zoospores,  and  the  idea  has  been  expressed  that  they 
stand  for  the  cooperative  union  of  many  hundreds  of  zoospores 
(energids)  represented  by  the  nuclei  and  their  respective  pairs  of 
cilia.  And  this  explanation  of  the  zoospore  of  Vaucheria  is  a 
part  of  a  broad  view,  formerly  very  largely  held,  that  the 
ccenocyte  is  an  assemblage  of  energids  (uninucleate  masses  of 
protoplasm)  cooperating  in  a  fused  structure. 

The  theory  of  the  cooperative  association  of  energids  in  a 
ccenocyte  (Sachs)  has  been  very  much  modified.  While  the 
nucleus  and  some  other  organs  of  the  cell,  such  as  groups  of 
cilia,  plastids,  etc.,  are  homologous  with  the  same  structures  in 
uninucleate  cells  nevertheless  the  behavior  of  the  ccenocyte  is 
not  the  same  as  a  group  of  cooperating  protoplasmic  units.  The 
ccenocyte  reacts  to  the  usual  stimuli  in  precisely  the  same  man- 
ner as  a  uninucleate  cell,  and  must  be  regarded  as  physiologi- 
cally presenting  no  peculiarities  over  the  latter  structure  except- 
ing those  of  an  increased  bulk  of  protoplasm  demanding  a  greater 
number  of  nuclei  for  its  metabolic  processes.  The  most  impor- 
tant contribution  presented  by  the  ccenocyte  to  our  knowledge 
of  the  physiology  of  the  cell  is  the  establishment  of  the  plasma 
membrane  as  the  region  of  the  protoplasm  responsive  to  the 
stimuli  that  determine  the  form  assumed  in  growth.  The  con- 
stant shifting  of  the  nuclei  and  plastids  in  the  movement  of  the 


750  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

granular  protoplasm  eliminates  them  as  structures  immediately 
concerned  with  the  form  of  a  cell  or  organ  thus  limiting  their 
functions  more  especially  to  metabolism. 

6.     The  Ccenogamete. 

The  cxnogamete  is  a  multinucleate  sexual  cell.  The  name 
was  first  applied  by  the  author  (Davis,  :  oo,  p.  307)  to  the 
remarkable  multinucleate  eggs  of  Albugo  bliti,  and  the  concep- 
tion has  been  considerably  extended  since,  as  explained  in  his  later 
writings  on  Saprolegnia  (Davis,  :  03,  p.  320-331)  and  on  "The 
relationships  of  sexual  organs  in  plants"  (Davis,  :  04^).  Ste- 
vens ('99)  discovery  of  the  multinucleate  eggs  of  Albugo  bliti 
opened  a  field  of  research  that  has  been  greatly  extended  in  the 
past  four  years  and  which  is  likely  to  yield  very  important  con- 
clusions on  the  relationships  and  evolution  of  the  Phycomycetes 
and  Ascomycetes.  Conditions  similar  to  Albugo  bliti  were 
reported  the  following  year  by  Harper,  :  oo£,  for  Pyronema,  and 
several  later  papers  have  described,  with  greater  or  less  fullness, 
the  structure  and  behavior  of  ccenogametes  in  some  other  Asco- 
mycetes, types  of  the  Peronosporales  (species  of  Albugo)  and  in 
the  Mucorales. 

We  shall  not  discuss  the  details  of  these  investigations  with 
their  bearings  upon  the  problems  of  phylogeny  as  this  has 
become  a  very  complicated  subject  and  is  treated  elsewhere 
(Davis,  :  04  a-b~),  but  merely  describe  the  structure  and  behavior 
of  ccenogametes  so  far  as  they  are  known  to  us. 

Stevens  and  Harper  both  found  that  the  multinucleate  female 
cell  of  Albugo  bliti  and  Pyronema  was  fertilized  by  the  introduc- 
tion of  a  large  number  of  nuclei  from  the  antheridium.  These 
sexual  nuclei  paired  off  and  fused,  a  male  with  a  female,  in  the 
common  mass  of  cytoplasm  so  that  the  fertilized  cell  finally  con- 
tained a  large  number  of  fusion  nuclei.  A  similar  history  was 
reported  later  by  Stevens  (:oi),  in  Albugo  portulacae  and  Albugo 
tragopogonis .  These  events  have  been  so  thoroughly  studied 
that  we  know  the  processes  of  fertilization  in  the  above  forms  as 
well  perhaps  as  for  any  plant  type. 

The    structure    and    especially  the  nuclear   history  of    other 


No.  454-]  STUDIES   ON   THE   PLANT  CELL.  751 

coenogametes  is  less  perfectly  understood.  The  multinucleate 
character  of  the  fusing  gametes  is  well  known,  but  the  later  dis- 
tribution and  fate  of  the  sexual  nuclei  has  not  been  followed,  and 
it  is  by  inference  that  we  believe  these  coenogametes  to  behave 
in  essentially  the  same  manner  as  those  of  Albugo  and  Pyronema. 

Coenogametes  fall  into  two  classes  according  as  they  involve 
all  of  the  protoplasm  contained  within  the  mother-cell  or  only  a 
portion  of  such  protoplasm.  The  first  group  probably  represents 
the  simplest  and  most  primitive  conditions. 

Ccenogametes  of  the  first  class  are  found  in  the  Mucorales 
(Gruber  :oi)  and  in  the  Gymnoasceas  (Dale,  :O3).  In  these 
types  the  entire  contents  of  the  terminally  formed  sexual  cells 
unite  to  produce  the  zygospore  in  the  former  group  and  the 
fertilized  ascogonium  in  the  latter,  from  which  arises  the  system 
of  ascogenous  hyphse. 

Coenogametes  of  the  second  class  contain  only  a  portion  of 
the  protoplasm  in  the  mother-cell  which  is  usually  a  terminal 
structure.  The  protoplasm  that  is  not  involved  in  the  cceno- 
gamete  proper  generally  bears  some  important  relation  to  the 
sexual  element.  Thus  the  periplasm  of  the  Peronosporales 
assists  in  the  formation  of  the  wall  of  the  oospore  and  the  con- 
jugation tube  of  Pyronema  becomes  the  path  through  which  the 
contents  of  the  antheridium  enters  the  ascogonium.  But  in 
some  forms  the  superfluous  protoplasm  is  merely  cut  off  from 
the  coenogamete  as  a  sterile  cell  (Monascus).  In  Albugo  and 
Pyronema  the  sterile  and  fertile  portions  of  the  protoplasm  are 
so  closely  associated  that  the  mother-cell  really  acts  as  a  whole, 
very  much  as  the  simplest  types  of  coenogametes  which  shows 
the  close  relationships  between  the  two.  Moreover  the  anthe- 
ridia  of  these  forms  are  types  of  coenogametes  almost  as  simple 
as  those  of  the  molds  or  the  Gymnoasceae. 

The  coenogamete  is  a  type  of  sexual  cell  unknown  in  the 
animal  kingdom  and  among  plants  is  probably  restricted  to  the 
Phycomycetes  and  Ascomycetes.  The  problems  of  its  homol- 
ogies  and  origin  are  very  interesting. 

The  simplest  types  of  cosnogametes  (Mucorales  and  Gymno- 
asceas) are  cells  situated  at  the  ends  of  filament's  in  the  same 
position  as  the  sexual  organs  of  the  Siphonales.  The  mother- 


752  THE   AMERICAN  NATURALIST.  [VOL.  XXXVIII. 

cells  of  the  more  complicated  coenogametes  (oogonia  and  anthe- 
ridia)  are  also  terminal  cells.  All  of  these  sexual  organs  are 
multinucleate.  In  the  Siphonales  (Vaucheria  excepted)  all  of 
the  nuclei  are  functional  gamete  nuclei.  This  is  also  true  of 
simplest  types  of  coenogametes,  but  in  the  more  complicated 
forms  (Albugo,  Pyronema,  etc.)  large  numbers  of  the  nuclei 
degenerate  or  fail  to  function  sexually  in  sterile  accessory  re- 
gions of  the  protoplasm.  The  same  conditions  of  sexual  degen- 
eration are  also  found  in  the  oogonia  of  Vaucheria  (Davis,  :  04) 
and  Saprolegnia  (Davis,  :O3).  The  agreement  of  all  of  the 
structures  mentioned  above  in  structure  and  protoplasmic  behav- 
ior seems  to  establish  beyond  question  their  common  homology. 
The  problems  of  the  origin  of  the  coenogametes  are  very 
difficult  with  the  meager  evidence  at  hand.  The  author  believes 
that  the  simplest  types  have  probably  been  derived  from  struc- 
tures like  the  sexual  organs  of  the  isogamous  Siphonales,  which 
structures  gave  up  the  habits  of  forming  uninucleate  gametes 
and  acting  as  coenocytic  units  became  multinucleate  sexual  ele- 
ments. A  physiological  development  very  similar  to  such  a 
change  must  have  taken  place  in  Peronospora  and  some  species 
of  Pythium  when  their  conidia  ceased  forming  zoospores  and 
took  the  habit  of  germinating  directly  by  a  tube.  This  view 
regards  the  ccenogamete  as  a  coenocyte  derived  from  a  proto- 
plasmic structure  that  at  one  time  produced  a  large  number  of 
independent  sexual  elements,  represented  in  the  ccenocyte  by  the 
numerous  nuclei.  Whether  the  higher  types  of  coenogametes 
(Albugo,  Pyronema,  etc.)  have  developed  directly  from  the  sim- 
pler forms  or  from  levels  of  the  heterogamous  algae,  such  as  are 
illustrated  by  Vaucheria,  are  very  complicated  problems  that  can- 
not be  treated  here.  They  with  other  topics,  mentioned  above, 
have  been  considered  in  recent  papers  of  the  author  (Davis,  :  03, 
;O4#,  104^).  Coenogametes  are  proving  to  be  among  the  most 
interesting  types  of  sexual  cells  in  plants  and  research  in  this 
field  is  likely  to  prove  very  fruitful  of  results. 


No.  454-]  STUDIES   ON   THE    PLANT   CELL.  753 

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and  i 14. 
DALE. 

:03.     Observations  on  the  Gymnoasceae.     Ann.  of  Bot.  17,  571. 
DANGEARD. 

'99.     Memoire  sur  les  Chlamydomonadinees  ou  1'histoire  d'une  cellule. 

LeBot.  VI,  65. 
DANGEARD. 

'01.     Etude  sur  la  structure  de  la  cellule  et  ses  functions,  Le  Polytoma 

uvella.     Le  Bot.  VIII,  5. 
DAVIS. 

'  99.     The  spore  mother-cell  of  Anthoceros.     Bot.  Gaz.  28,  89. 
DAVIS. 

:OO.     The  fertilization  of  Albugo  Candida.     Bot.  Gaz.  29,  297. 
DAVIS. 

:01.     Nuclear  studies  in  Pellia.     Ann.  of  Bot.  15,  147. 
DAVIS. 

:03.     Oogenesis  in  Saprolegnia.     Bot.  Gaz.  35,  233  and  320. 
DAVIS. 

:04<?.     Oogenesis  in  Vaucheria.     Bot.  Gaz.  38,  81. 
DAVIS. 

:  04<$.     The  relationships  of  sexual  organs  in  plants.     Bot.  Gaz.  38,  243. 


No.  454-]  STUDIES   ON   THE  PLANT  CELL.  755 

Dixox. 

'94.     Fertilization  of  Pinus  sylvestris.     Ann.  of  Bot.  8,  21. 

DUGGAR. 


'  99.     On  the  development  of  the  pollen  grain  and  embryo-sac  in  Bignonia 

venusta.     Bull.  Tor.  Bot.  Club,  26,  89. 
DUGGAR. 

:00.     Studies  in  the  development  of  the  pollen  grain   in   Symplocarpus 

foetidus  and  Peltandra  undulata.     Bot.  Gaz.  29,  81. 
ERNST. 

:  02.     Chromosomenreduction,  Entwickelung  des  Embryosackes   und  Be- 
fruchtung   bei    Paris    quadrifolia    L.  und    Trillium    grand iflorum 
Salisb.     Flora,  91,  i . 
FAIRCHILD. 

'  94.     Ein  Beitrag  zur    Kenntniss    der  Kerntheilung  bei    Valonia  utricu- 

laria.     Ber.  d.  deut.  bot.  Gesell.  12,  331. 
FARMER. 

'  93.     On  nuclear  division  in  the  pollen  mother-cells  of  Lilium  martagon. 

Ann.  of  Bot.  8,  392. 
FARMER. 

'  94.     Studies  in  Hepaticae  :     On  Pallavicinia    decipiens    Mitten.     Ann. 

of  Bot.  8,  35. 
FARMER, 

'  95a.     Spore  formation  and  karyokinesis  in  Hepaticae.     Ann.  of   Bot.  9, 

363- 
FARMER. 

95<£.     On  spore  formation  and  nuclear  division  in    the  Hepaticae.      Ann. 

of  Bot.  9,  469. 
FARMER. 

'  95c.     Further   investigations   on    spore   formation  in  Fegatella  conica. 

Ann.  of  Bot.  9,  666. 
FARMER. 

'  95d.     Ueber  Kerntheilung  in  Lilium-antheren,  besonders  in    Bezug  auf 

die  Centrosomenfrage.     Flora,  80,  56. 
FARMER. 

:  01.     The     quadripolar   spindle     in    the    spore    mother-cell    of    Pellia 

epiphylla.     Ann.  of  Bot.  15,  431. 
FERGUSON. 

:  01^.     The    development  of  the  egg  and  fertilization  in  Pinus  strobus. 

Ann.  of  Bot,  15,  435. 
FRYE. 

:01.     Development  of  the  pollen  in    some    Asclepiadaceae.     Bot.  Gaz. 
32,  325. 

GAGNER. 

:  02.     The  development  of  the  pollinium  and    sperm   cells  in  Asclepias 
Cornuti,  Decaise.     Ann.  of  Bot.  16,  123. 


756  THE  AMERICAN  NATURALIST.  [VOL.  XXXVI IK 

GREGOIRE. 

'  99.     Les  cineses  polliniques  chez  les  Liliace'es.     La  Cellule  16,  325. 
GRUBEK. 

:  01.     Ueber  das  Verhalten  der  Zellkerne  in  den  Zygosporen  von  Sporo 
dinia  grandis  Link.     Ber.  d.  deut.  hot.  Gesell.  19,  51. 

GUIGNARD. 

'91.     Nouvelles  e'tudes  sur  la  fecondation.     Ann.  d.  Sci.  Nat.  Bot.  VII, 

14,  163. 
GUIGNARD. 

'  97.     Les  centres    cine'tiques  chez  les  ve'ge'taux.     Ann.  d.  Sci.  Nat.  Bot. 

VIII,  6,  177. 
GUIGNARD. 

'98.     Centrosomes  in  Plants.     Bot.  Gaz.  25,  158. 
HARPER. 

:  QQb.     Sexual  reproduction  in  Pyronema  confluens  and  the  morphology 

of  the  ascocarp.     Ann.  of  Bot.  14,  321. 
HIRASE. 

'  94.     Notes     on    the    attractions-spheres  in    the    pollen-cells  of  Ginko 

biloba.     Bot.  Mag.  Tokyo  8,  359. 
HIRASE.  « 

'97.     Untersuchungen  iiber  das  Verhalten  des  Pollens  von  Ginko  biloba. 

Bot.  Centb.  69,  33. 
HIRASE. 

'  98.     Etude  sur  la  fecondation  et  1  'embryogenie  du  Ginko  biloba.    Jour. 

Coll.  Sci.  Imp.  Tokyo,  12,  103. 
IKENO. 
'  98a.     Zur  Kenntniss    des    sogenanten    centrosomahnlichen  Korpers  im 

Pollenschlauch  der  Cycadeen.     Flora  85,  15. 
IKENO. 

'  98(5.     Untersuchungen  iiber   die  Entwickelung  der   Geschlechtsorgane 
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IKENO. 
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Ann.  d.  Sci.  Nat.  VIII,  13,  305. 
IKENO. 

:  03.  Beitrage  zur  Kenntniss  der  pflanzlichen  Spermatogenese :  Die 
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Centb.  15,  65. 

JUEL. 

'  97.     Die   Kerntheilung    in    den    Pollenmutterzellen   von    Hemerocallis 
fulva    und  die  bei  denselben    auftretenden    Unregelmassigkeiten. 
Jahrb.  f.  wiss.  bot.  30,  205. 
JUEL. 

:  00.  Beitrage  zur  Kenntniss  der  Tetradentheilung.  Jahrb.  f .  wiss.  Bot. 
35,  626. 


No.  454-]  STUDIES   ON   THE   PLANT  CELL.  757 

KARSTEN. 

'  92.     Beitrage  zur  Entwickelungsgeschichte  der  Gattung  Gnetum.     Bot. 

Zeit.  50,  205,  221  and  237. 
KARSTEX. 
'  93.     Zur  Entwickelungsgeschichte  der  Gattung  Gnetum.     Cohns    Beit. 

z.  Biol.  d.  Pflan.  6,  337. 
KLEBAHX. 

'  92.     Die  Befruchtung  von  Oedogonium  boscii.     Jahrb.  f.  wiss.  Bot.  24, 

235- 
KLEMM. 

'  93.     Ueber  Caulerpa  prolifera.     Flora,  77,  460. 
KLEMM. 

'  94.     Ueber  die  Regenerationsvorgange   bei    den    Siphonaceen.     Flora, 

78,  19. 
LAXD. 

:02.     A  morphological  study  of  Thuja.     Bot.  Gaz.  34,  249. 
LAWSON. 

'  98.     Some  observations  on  the  development  of  the  karyokinetic  spindle 
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LAWSON. 

:  00.     Origin  of  the  cones  of  the  multipolar  spindle  in  Gladiolus.     Bot. 

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LOTSY. 

'  99.     Contributions  to  the  life  history  of  the  genus   Gnetum.     Ann.  Jar. 

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MIYAKE. 
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:  03^.     Contribution   to   the   fertilization   and    embryogeny  of  Abies  bal- 

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:  03.  The  mitoses  in  the  spore  mother-cell  of  Pallavicinia.  Bot.  Gaz.  36r 
384- 

MOTTIER. 

'  97.  Beitrage  zur  Kenntniss  der  Kerntheilung  in  den  Pollenmutterzellen 
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'98.  Ueber  das  Verhalten  der  Kerne  bei  der  Entwickelung  des  Embryo- 
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31,  125. 


758  THE  AMERICAN  NATURALIST.   [VOL.  XXXVIII. 

MOTTIER. 

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MURRILL. 

:00.     The  development  of  the  archegonium  and  fertilization  in  the  hem- 
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'87.     Experimented  Untersuchungen  uber  das  Wachsthum  der  Zellmem- 

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'B8a.     Ueber   die    Function    der    Zellstoffasern    der   Caulerpa    prolifera. 

Arbeit,  a.  d.  bot.  Inst.  WUrz.  3,  459. 
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'88<£.     Ueber  den  Einfluss  der  Lage  auf  die  morphologische  Ausbildung 

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'95.     Ueber  die    Entwickelung  die    Sexualorgane  be  Vaucheria.   Flora, 

80,  388. 
OLTMANNS. 

'98.     Die    Entwickelung   der    Sexualorgane    bei    Coleochaete    pulvinata. 
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OSTERHOUT. 

'97.     Ueber   Entstehung  der  karyokinetischen    Spindel  bei    Equisetum. 

Jahrb.  f.  wiss.  Bot.  30,  159. 
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'97.     The  formation  of    sexual  nuclei    in   Lilium  martagon :    Spermato- 

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'9Ba.     The  fertilization  of  Onoclea.     Ann.  of  Bot.  12,  261. 


No.  454.]  STUDIES   ON    THE  PLANT  CELL.  759 

SHAW. 

'98/5.     Ueber  die   Blepharoplasten   bei  Onoclea  und    Marsilia.     Ber.  d. 

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STEVENS,  F.  L. 

'99.     The  compound  oosphere  of  Albugo  bliti.     Bot.  Gaz.  28,  149. 
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'98a.     Ueber    Chromosomtheilung   bei    der    Sporenbildung   der    Fame. 

Ber.  d.  deut.  bot.  Gesell.  16,  261. 
STEVENS,  W.  C. 

'98(5.     The  behavior  of  kinoplasm  and  the  nucleolus  in  the  division  of  the 
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77- 
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'72.     Die  Coniferen  und  die  Gnetaceen. 
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'80.     ZeHbildung  und  Zelltheilung.     Jena. 
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'92.     Schwarmsporen,    Gameten,    pflanzlichen    Spermatozoiden.      Hist. 

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'95.     Karyokinetische  Probleme.     Jahrb.  f.  wiss.  Bot.  28,  151. 
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'95a.     New  or  peculiar  aquatic  fungi :    Monoblepharis.     Bot.  Gaz.  20, 

433- 
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'95^.     New  or  peculiar  aquatic  fungi :  2,  Gonapodya  and  Myrioblepharis. 

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'99.     The  process  of  fertilization   in  Aspidium  and  Adiantum.     Trans. 
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760  THE   AMERICAN  NATURALIST.    [VOL.  XXXVIII. 

TlMBERLAKE. 

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'99.     On  the  eye-spot  and  flagellum  in  Euglena  viridis.     Jour.  Linn.  Soc. 

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WEBBER. 

'97#.     Peculiar  structures  occurring  in  the  pollen  tube  of  Zamia.     Bot. 

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WEBBER. 

'97(5.     The  development  of  the  antherozoids  of  Zamia.     Bot.  Gaz.  24,  16. 
WEBBER. 

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of  Ginko.     Bot.  Gaz.  24,  225. 
WEBBER. 

:01.     Spermatogenesis  and  fecundation  of  Zamia.     Bu.  Plant  Ind.  U.  S. 

Dept.  Agri.  Bull.  2. 
WIEGAND. 

'99.     The  development  of  the  microsporangium  and  microspores  in  Con- 

vallaria  and  Potomogeton.     Bot.  Gaz.  28,  328. 
WILLIAMS,  CLARA  I. 

'99.     The  origin  of  the  karyokinetic  spindle  in  Passiflora  coerulea.     Proc. 

Cal.  Acad.  Sci.  Bot.  1,  189. 
WILSON. 

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ZACHARIAS. 

'87.     Beitrage  zur  Kenntniss  des  Zellkerns  und  der  Sexualzellen.     Bot. 
Zeit.  45,  345. 

ZlMMERMANN. 

'93,  '94.     Sammel-Referate    aus    dem   Gesammtgebiete  der  Zellenlehre. 
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ZlMMERMANN. 

'96.     Die    Morphologic    und    Physiologic   des    Pflanzlichen    Zellkernes. 
Jena. 

( To  be  continued.} 


VOL.  XXXIX,  No.  460  APRIL,  1905 

THE 

AMERICAN 
NATURALIST 


A    MONTHLY   JOURNAL 

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Page 
I.    Birds  of  the  Isle  of  Pines  .        0.  BANGS  and  W.  R.  ZAPPEY      179 

II.    Studies  on  the  Plant  Cell.-  V                ...             .    DR.  B.  M.  DAVIS      21T 
III-  Correspondence  .  269 


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J.  H.  COMSTOCK,  S.B.,  Cornell  University,  Ithaca. 
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ALES  HRDLICKA,  M.D.,   U.S.  National  Museum,  Washington. 
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ISRAEL  C.  RUSSELL,  LL.D.,  University  of  Michigan,  Ann  Arbor. 
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s 
STUDIES    ON    THE    PLANT    CELL.  — V. 

BRADLEY  MOORE  DAVIS. 

SECTION  IV.     CELL  UNIONS  AND  NUCLEAR  FUSIONS  IN 

PLANTS. 

THE  forms  of  cell  unions  and  nuclear  fusions  in  plants  fall 
into  two  groups  :  (i)  those  which  obviously  have  no  sexual  sig- 
nificance attached  to  them,  and  (2)  those  which  are  evidently 
sexual  acts.  But  apart  from  these  simple  divisions  there  are 
some  very  interesting  conditions  in  which  it  is  far  from  easy  to 
determine  whether  certain  events  have  a  sexual  significance  either 
physiologically  or  phylogenetically.  The  real  test  of  such  prob- 
lems should  lie  in  the  evolutionary  history  of  the  processes 
involved,  for  every  sexual  condition  in  plants  has  probably 
developed  in  obedience  to  the  same  physiological  demands  and 
in  an  essentially  similar  manner.  However,  we  cannot  apply  the 
evolutionary  test  in  many  cases  where  we  have  little  evidence  of 
the  developmental  history  of  the  group  and  such  forms  must  rest 
for  the  present  as  unsolved  problems.  We  shall  treat  them  in 
special  connections  later  in  the  paper. 

The  material  of  this  section  will  be  presented  under  the  fol- 
lowing heads : — 

1.  Protoplasmic    connections  between  cells  (plasmodesmen). 

2.  Sexual  cell  unions  and  nuclear  fusions. 

3.  Asexual  cell  unions  and  nuclear  fusions. 

i.    Protoplasmic  Connections  between  Cells  (Plasmodesmen). 

It  has  been  known  for  a  great  many  years  that  the  walls 
between  the  cells  in  some  plant  tissues  and  more  especially 
between  the  cells  of  filaments  in  certain  thallophytes  were 
crossed  by  delicate  strands  of  protoplasm  so  that  contiguous  pro- 
toplasts were  not  entirely  separated  from  one  another.  This  fact 

217 


2l8  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

offers  at  once  many  interesting  possibilities  of  explaining  the 
close  association  of  many  cells  and  tissues,  not  alone  in  delicate 
dynamic  interrelations  but  even  in  the  exchange  and  distribution 
of  food  material  and  other  products  of  metabolism.  It  makes 
possible  the  conception  of  the  plant  body  as  a  finely  adjusted 
community  of  protoplasts  intimately  and  sensitively  related  to  a 
great  degree  in  all  parts,  a  view  very  different  from  the  old  idea 
of  a  cell  republic.  As  might  be  expected,  these  speculative 
possibilities  were  conceived  and  expressed  by  such  leaders  as 
Hofmeister,  Nageli,  Sachs,  and  Strasburger  long  before  the 
detailed  study  of  protoplasmic  connections  gave  the  mass  of  evi- 
dence upon  which  have  been  based  the  more  elaborate  concep- 
tions of  recent  years. 

The  most  obvious  protoplasmic  connections  between  cells  may 
be  found  in  the  thallophytes  where  as  in  the  Rhodophyceae, 
Volvox,  and  in  certain  fungi,  the  cells  in  younger  structures  may 
be  observed  under  comparatively  low  magnification  to  be  united 
by  strands  of  protoplasm  so  broad  as  to  quite  exclude  them  from 
the  category  of  fibrillae.  Some  of  these  structures  are  so  con- 
spicuous that  it  is  surprising  that  more  was  not  made  of  them  by 
early  writers  and  that  they  have  not  been  more  extensively 
investigated  recently.  The  greater  part  of  the  papers  have 
been  on  the  very  difficult  phase  of  the  subject,  the  structure  of 
pores  and  pits  in  the  tissues  of  higher  plants.  The  literature 
treating  of  protoplasmic  connections  is  too  extensive  to  be  given 
detailed  treatment  in  the  compass  of  this  paper.  The  best 
review  of  the  subject  is  that  of  Strasburger  (:  01),  supplemented 
by  the  more  recent  paper  of  Kienitz-Gerloff  ('.02). 

The  earlier  papers  on  the  protoplasmic  connections  in  higher 
plants,  following  the  establishment  of  perforations  of  sieve-plates 
by  Sachs  and  Hanstein,  appeared  during  the  years  just  preceding 
and  following  1880.  Thus  Tangl  ('79-'8i)  described  very  clearly 
the  communications  between  the  endosperm  cells  of  StrycJinos 
mix  vomica  and  Phoenix  (see  Fig.  16,  a).  Tangl  noted  the  resem- 
blance of  the  complex  of  connecting  threads  to  the  arrangement 
of  spindle  fibers  associated  with  the  simultaneous  division  of  the 
protoplasm  in  the  endosperm  but  was  cautious  in  assuming  a 
relationship,  suggesting  that  the  resemblance  might  be  super- 
ficial. 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  219 

Strasburger  ('82,  p.  246)  discussed  the  permeability  of  cell 
walls  and  Gardiner  ('88)  gave  a  general  treatment  of  the  subject 
without,  however,  any  figures  to  illustrate  his  -conclusions. 
Gardiner  discovered  for  a  large  number  of  forms  in  a  wide 
variety  of  families  that  the  pit  membranes  were  frequently 
pierced  by  protoplasmic  fibrils  and  that  in  some  cases  the  fibrils 
traversed  the  entire  thickness  of  the  cell  wall.  A  more  detailed 
study  with  better  methods,  supplementing  his  former  work  and 
accompanied  by  figures,  was  published  by  Gardiner,  in  1898, 
this  paper  forming  an  important  contribution  to  the  subject. 
Gardiner  (:  oo)  announced  himself  strongly  in  favor  of  the  view 
that  the  protoplasmic  connections  between  cells  were  derived 
from  spindle  fibers  of  nuclear  figures  concerned  with  each  cell 
division,  a  possibility  which  had  been  suggested  by  previous 
writers  (Tangl,  '79-'8i  ;  Russow,  '83). 

Kienitz-Gerloff  ('91)  gave  an  excellent  account  of  the  proto- 
plasmic connections  in  a  number  of  forms,  some  of  them 
pteridophytes,  but  especially  for  Viscum  album,  and  followed  the 
history  of  the  wall  formation,  showing  that  the  spindle  fibers 
disappeared  completely  before  the  development  of  the  connect- 
ing strands  of  protoplasm.  Kuhla  (:  oo)  followed  Kienitz- 
Gerloff  with  more  extended  studies  on  the  same  form,  Viscum 
album,  tracing  the  protoplasmic  fibrils  between  the  cells  in  all 
the  chief  tissues  and  establishing  the  protoplasmic  connections 
throughout  the  individual  to  an  extent  that  was  not  known 
before.  Hill  (:oi)  described  the  structure  of  the  sieve-tubes  of 
Pinus,  dealing  especially  with  the  formation  of  callus  and  the 
conversion  of  the  connecting  threads  of  protoplasm  into  strings 
of  slime.  An  excellent  review  is  also  given  of  the  work  of 
Russow  and  others,  particularly  upon  sieve-tubes.  Kohl  ('97) 
describes  clearly  protoplasmic  connections  between  the  cells  of 
moss  leaves. 

A  classification  of  protoplasmic  connections  was  suggested 
by  Kohl  (:oo)  who  distinguished  bet  ween  the  solitary  state  when 
each  fibril  pierces  the  cell  wall  independently  of  its  neighbors 
(Fig.  1 6,  a  and  b)  and  a  grouped  condition  when  a  number  of 
fibers  arise  close  together  at  the  bottom  of  a  pit  and  pierce  the 
pit-membrane  or  middle  lamella  in  a  spindle-shaped  arrangement, 


22O 


THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 


reminding  one  of  the  central  spindle  of  a  mitotic  figure  (Fig. 
1 6,  c).  In  general  the  two  types  of  protoplasmic  connections  are 
not  found  together  in  the  same  cell  or  tissue. 

A  new  point  of  view  was  introduced  into  the  discussion  by 
the  very  important  paper  of  Strasburger,  in  1901.  He  consid- 
ered the  protoplasmic  connections  as  sufficiently  clearly  differ- 
entiated structures  to  rank  as  organs  of  the  cell  and  proposed 
for  them  the  name  plasmodesmen.  Strasburger  in  agreement 


FIG.  16.  —  Protoplasmic  connections  between  cells  of  plants,  a,  endosperm  cells  of  Strych- 
nos  nux  vomica  ;  6,  details  of  the  solitary  fibers  in  the  same  form,  (m)  middle  lamella ;  c, 
grouped  fibers  at  bottom  of  pit  in  endosperm  of  Phytelephas  and  crossing  the  pit  mem- 
brane in  a  spindle-shaped  figure :  d,  cell  connections  around  the  sporophytic  portion  of  a 
developing  cystocarp  of  Champia,  (s)  sporophytic  elements ;  e,  fibers  between  cells  of 
Cladophora;  f,  cell  connections  around  the  ascogenous  elements  in  Laboulbenia ;  g, 
clamp  connections  in  Pleurotus  (a,  after  Tangl,  *7q-'8i;  b  and  c,  Kohl,  :oo;  d,  Davis, 
'96  b;  e,  Kohl,  :  02  ;  f,  Thaxter,  '96  ;  g,  Meyer,  :o2). 

with  Kienitz-Gerloff  opposed  the  view  that  the  plasmodesmen 
were  in  any  way  derived  from  or  related  to  the  spindle  fibers 
associated  with  the  formation  of  cell  plates.  He  believed  them 
to  be  developments  of  the  outer  plasma  membrane  as  he  like- 
wise considers  the  cilia  in  certain  zoospores  (see  account  of 
zoospore  and  sperm  in  Section  III,  Amer.  Nat.  vol.  38,  pp.  571, 
576,  1904).  Strasburger  also  holds  that  pores  are  formed  in  the 
cell  walls  by  the  fermative  activities  around  plasmodesmen.  A 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  221 

recent  short  paper  by  Michniewicz  (:  04)  describes  clearly  the 
plasmodesmen  in  Lupinus,  especially  in  their  relation  to  masses 
of  intercellular  protoplasm  which  are  discussed  at  the  end  of 
this  portion  of  the  section. 

It  is  not  clear  whether  all  protoplasmic  connections  may  be 
considered  in  the  same  class,  as  Strasburger  would  have  us 
believe,  or  whether  there  may  not  be  some  confusion  between 
the  broader  cell  connections  which  are  especially  conspicuous  in 
the  thallophytes  and  certain  tissues  (sieve-tubes,  laticiferous 
vessels),  and  the  delicate  protoplasmic  fibrils  (plasmodesmen)  so 
general  throughout  all  tissues  of  higher  plants.  As  is  well 
known,  the  cells  in  actively  growing  regions  of  the  red  algae  are 
connected  by  broad  strands  of  protoplasm  that  are  obviously 
left  by  the  cleavage  furrow  which  constricts  the  protoplasm  of 
daughter  cells  but  does  not  entirely  separate  them.  These  open- 
ings may  become  partially  blocked  in  older  portions  of  the  plant 
by  the  deposition  of  material  so  that  the  connections  are  finally 
fibrillar  but  they  frequently  remain  open  for  long  periods,  par- 
ticularly in  regions  where  the  nutritive  processes  are  active  as 
during  the  development  of  cystocarps.  At  this  time  new 
fusions  may  be  developed  between  neighboring  cells  (auxiliary 
cells)  so  that  they  become  connected  in  an  elaborate  network 
around  the  cells  or  filaments  (sporophytic)  that  develop  the  car- 
pospores  (Fig.  16,  d).  The  Phaeophyceae  also  furnish  frequent 
illustrations  of  connecting  fibrils  especially  in  the  Fucales  and 
Laminariales  where  the  cells  of  internal  filaments  are  sometimes 
connected  by  conspicuous  strands.  Certain  elongated  filaments 
which  traverse  the  central  region  of  the  larger  brown  algae  show 
a  complicated  group  of  fibrils  that  strikingly  resembles  the  pro- 
toplasmic connections  piercing  the  sieve-plates  of  higher  plants. 
Broad  protoplasmic  connections  are  conspicuous  between  the 
cells  of  some  of  the  filamentous  Cyanophycese  (Stigonema, 
Tolypothrix)  and  in  the  Chlorophyceae  have  been  reported  for 
some  species  of  Cladophora  (Kohl,  :  02  ;  Fig.  16,  e)  and  for 
Chsetopeltis,  one  of  the  Mycoidese.  They  do  not  seem  to  be 
present  in  the  Conjugales  as  was  at  first  reported  by  Kohl 
('91)  whose  cells  show  a  great  degree  of  physiological  inde- 
pendence. In  Volvox,  studied  by  Meyer  ('96),  each  cell  of  the 


222  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

sphere  is  connected  with  its  neighbors  generally  by  six  strands 
of  protoplasm,  only  a  few  of  which  could  possibly  be  left  by  the 
successive  cell  divisions.  The  majority  must  have  developed  as 
outgrowths  from  the  plasma  membrane  of  the  cell. 

Numerous  instances  of  cytoplasmic  connections  among  the 
fungi  have  been  reported  by  many  authors.  A  general  review 
of  the  subject  is  presented  by  Kienitz-Gerloff  (:O2)  and  in  a 
lengthy  paper  of  Meyer  (:O2).  The  protoplasmic  connections 
fall  into  two  groups  :  ( i )  those  that  remain  in  the  center  of  the 
wall  after  a  cell  division,  and  (2)  the  lateral  unions  and  clamp 
connections  which  are  developed  entirely  independently  of  cell 
division.  Connections  of  the  first  type,  i.  e.,  those  between 
daughter  cells,  appear  to  be  very  general  in  the  Ascomycetes 
and  Basidiomycetes  and  are  essentially  similar  to  the  strands 
between  cells  of  the  Rhodophyceae.  They  are  especially  well 
illustrated  in  members  of  the  Laboulbeniacese  (Thaxter,  '96  ; 
see  Fig.  16,  f ).  In  the  second  group  are  the  clamp  connections 
(Fig.  1 6,  g),  characteristic  structures  of  the  tissues  of  fleshy 
forms  of  the  Basidiomycetes,  and  the  lateral  unions  between 
cells  of  closely  entangled  hyphse  which  are  well  known  in  a 
number  of  forms  and  have  been  followed  in  cultures  from  germi- 
nating spores.  It  is  probable  that  the  fusions  between  sporidia 
in  the  smuts  are  also  of  this  class,  although  De  Bary  and  others 
have  attached  sexual  significance  to  the  phenomenon  (especially 
as  illustrated  by  Tilletia).  Harper  ('99a)  has  studied  the  fusions 
of  the  conidia  of  Ustilago  and  finds  that  they  concern  the  cyto- 
plasm alone.  However,  Federley  (103-:  04)  has  reported  a 
nuclear  fusion  in  one  species  (Ustilago  tragopogonis  pratensis 
Pers.)  but  states  that  others  agree  with  Harper's  account. 
Extensive  experiments  of  Brefeld  have  shown  that  the  fusions 
of  sporidia  depend  largely  upon  the  character  of  the  nutrient 
media  and  are  less  likely  to  occur  when  the  conditions  are  favor- 
able. He  considers  the  fusions  as  purely  vegetative  processes 
comparable  to  the  unions  of  germ  tubes  of  spores  (e.  g.,  Nec- 
tria,  Sclerotinia,  Rhyparomyces,  etc.)  into  a  common  mycelium 
and  to  the  connections  between  hyphae  of  Basidiomycetes. 
Recent  studies  of  Blackman  (104  a)  indicate  also  that  sexual 
processes  should  not  be  expected  at  this  period  in  the  life  his- 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  223 

tory  of  smut  or  rust.  One  of  the  best  discussions  of  cell 
fusions  in  the  fungi  is  that  in  Harper's  paper  ('99  a),  noted 
above. 

Although  most  of  the  protoplasmic  connections  in  higher 
plants  are  of  the  fibrillar  character  there  are  some  notable  illus- 
trations of  broad  openings  between  cells,  even  more  conspicuous 
than  those  in  the  red  algae.  Such  may  be  found  in  the  pores  of 
sieve-plates  traversed  in  their  early  stages  by  strands  of  proto- 
plasm that  later  disappear,  and  even  better  illustrations  are  the 
unions  between  cells  composing  laticiferous  vessels.  But  the 
most  interesting  conditions  are  those  associated  with  the  nutri- 
tion of  the  eggs  of  certain  cycads.  Goroschankin  ('83)  first 
noted  for  the  cycads  pores  or  canals  in  the  egg-wall  of  Ceratoza- 
mia  and  described  communications  between  the  protoplasm  of 
the  enveloping  cells  of  the  jacket  and  the  egg.  The  subject  is 
closely  associated  with  the  explanation  of  the  proteid  vacuoles  in 
the  eggs  of  gymnosperms  which  Arnoldi  believed  to  be  nuclei 
that  had  migrated  from  the  surrounding  cells.  The  conclusions 
of  Arnoldi  have  not  been  sustained  (see  Sec.  Ill,  Amer.  Nat.,  vol. 
38,  pp.  591,  592,  1904)  but  the  presence  of  pores  in  the  egg-wall 
of  gymnosperms  is  likely  to  prove  very  general  with  further 
investigation.  A  recent  paper  by  Miss  Isabel  Smith  (:O4)  gives 
an  account  of  haustoria-like  processes  from  the  egg  of  Zamia 
which  pass  through  the  pores  of  the  egg-wall  into  the  cells  of 
the  jacket,  where  they  are  in  direct  contact  with  its  -protoplasm. 
These  pseudopodia-like  processes  of  the  egg  apparently  absorb 
material  from  the  cells  of  the  jacket  as  is  indicated  by  the  char- 
acter of  their  staining  and  the  streaming  movement  towards 
them  of  the  protoplasm  in  the  jacket  cells.  The  relation  of  the 
plasma  membrane  of  the  processes  from  the  egg  to  that  of  the 
jacket  cells  is  not  clear  but  probably  they  are  merely  in  contact 
and  not  in  open  communication.  The  ovules  of  cycads  seem  to 
offer  an  especially  favorable  subject  for  the  study  of  pore  forma- 
tion and  the  intimacy  of  protoplasmic  connections  between  cells. 

It  seems  very  clear  that  the  cytoplasmic  connections  in  the 
Rhodophyceae,  Volvox,  fungi,  and  between  the  egg  and  jacket 
cells  of  cycads  involve  very  much  more  substance  than  is  gen- 
erally present  in  the  delicate  fibrillae  of  higher  plants.  Meyer 


224  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

(:O2,  pp.  167,  168)  seems  justified  in  emphasizing  their  resem- 
blance to  pseudopodia  rather  than  to  any  other  structure  of  the 
cell.  If  they  should  finally  be  connected  by  intergradations 
with  the  exceedingly  fine  plasmodesmen  of  Strasburger,  there 
would  stand  at  one  end  of  the  series  structures  so  thick  as  to 
be  composed  of  a  plasma  membrane  containing  much  cytoplasm 
in  the  interior  and  behaving  like  haustoria  or  pseudopodia  and 
at  the  other  end  delicate  fibrillae.  Viewing  the  problem  of  their 
relationships  from  the  lower  plants  upwards,  it  is  very  difficult, 
if  not  impossible  to  follow  Strasburger's  theory  that  all  cytoplas- 
mic  connections  (plasmodesmen)  are  related  to  developments 
from  the  plasma  membrane  similar  to  cilia.  They  seem  to  be 
more  of  the  nature  of  processes  put  out  from  the  cytoplasm  and 
when  necessary  penetrating  cellulose  walls  probably  in  response 
to  chemotactic  stimuli  since  they  are  most  conspicuous  when 
metabolic  activities  are  obviously  important  (e.  g.,  nourish- 
ment of  the  egg  in  gymnosperms  and  sporophytic  generation 
of  the  red  algae). 

In  method  of  development  we  have  seen  that  protoplasmic 
connections  fall  into  two  classes:  (i)  those  that  represent  the 
incomplete  separation  of  daughter  cells,  and  (2)  those  that 
result  from  the  coming  together  or  fusion  of  protoplasmic  out- 
growths. The  types  of  the  first  group  are  always  in  the  be- 
ginning open  communications  which  later  may  become  largely 
or  wholly  closed  ;  types  of  the  second  group  may  result  in  broad 
cytoplasmic  fusions  (e.  g.,  many  fungi)  but  there  is  evidence 
that  in  many  cases,  especially  among  the  higher  plants,  the  two 
processes  only  come  in  contact  so  that  the  plasma  membranes 
are  applied  to  one  another  but  do  not  actually  unite.  It  does 
not  seem  probable  that  the  two  methods  of  development  or  the 
presence  or  absence  of  intimate  protoplasmic  union  indicate  a 
different  kind  of  structure.  They  are  more  likely  to  be  only 
varied  responses  to  the  demands  for  a  more  or  less  close  associa- 
tion of  neighboring  cells.  Broad  communications  are  especially 
characteristic  of  regions  where  there  is  evidently  an  extensive 
demand  for  the  nourishment  of  a  cell  or  tissue,  as  in  the  eggs  of 
the  cycads  or  the  cystocarp  of  the  red  algae. 

The  functions  of  protoplasmic  connections  are  probably  vari- 


No.  460.]  STUDIES   ON  PLANT  CELL — V.  225 

4 

ous.  It  is  evident  that  they  bind  the  whole  plant  body  into  a 
cell  complex  capable  of  very  delicate  interrelations.  It  is 
natural  that  physiologists,  Pfeffer  and  others,  should  .associate 
the  structures  with  the  phenomena  of  irritability  as  the  paths 
over  which  stimuli  may  be  transmitted  from  cell  to  cell  and 
tissue  to  tissue.  Several  writers  have  reported  their  presence  in 
unusual  numbers  in  irritable  structures  of  plants.  The  subject 
is  discussed  in  great  detail  by  Strasburger  (:oi,  p.  533). 

Besides  conducting  stimuli,  there  is  much  evidence  that 
material  may  be  transferred  in  solid  or  semifluid  form  by  the 
protoplasmic  connections  from  cell  to  cell  and  that  in  some 
instances  there  is  actually  a  movement  or  flow  of  protoplasm. 
It  is  even  known  that  nuclei  may  pass  from  cell  to  cell  through 
pores  in  the  wall,  especially  after  some  shock,  as  in  the  neigh- 
borhood of  wounds  (Miehe,  :oi),  or  when  temperature  is  sud- 
denly raised  (Schrammen,  :O2).  This  literature  and  other 
references  are  discussed  by  Koenicke  (:oi;  :O4).  A  flow  of 
protoplasm  between  neighboring  cells  of  hyphae  has  been 
reported  by  Reinhardt  ('92)  and  Charlotte  Ternetz  (:oo). 
That  nuclei  may  pass  through  very  small  space  is  shown 
in  the  development  of  spores  in  the  Basidiomycetes  and  in 
the  growth  of  haustoria  from  the  cells  of  hyphae  (Smith,  :  oo). 
There  are  many  forms  known,  especially  among  the  thallo- 
phytes,  where  the  communications  between  cells  are  so  broad 
as  to  admit  of  a  very  free  circulation  of  their  contents.  Such 
conditions  are  especially  well  illustrated  in  tissues  around  the 
developing  cystocarps  of  the  Rhodophyceae  and  the  ascocarp 
of  the  Ascomycetes,  both  structures  apparently  sporophytic  in 
charater  and  dependent  to  a  great  degree  upon  the  gametophyte 
as  a  host.  It  is  believed  that  the  vitality  of  protoplasm  in  sieve 
tubes,  whose  nuclei  have  degenerated  and  disappeared,  is  main- 
tained through  protoplasmic  connections  with  neighboring  cells 
and  especially  the  companion  cells,  when  present.  Of  course 
where  an  actual  circulation  of  protoplasm  is  established  between 
cells  or  tissues  there  is  made  possible  a  distribution  of  the 
products  of  metabolism  in  solid  form  that  is  very  different  from 
the  usual  diffusion  in  tissues  through  cell  walls  and  plasma  mem- 
branes. 


226  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

It  seems  probable  that  there  are  really  two  forms  of  proto- 
plasmic connections  between  cells  in  plants :  first,  those  so 
intimate  that  the  plasma  membranes  are  pierced  and  become 
continuous  openings  inclosing  a  strand  of  granular  cytoplasm 
within ;  and  second,  those  in  which  the  plasma  membranes  are 
merely  applied  to  one  another  without  open  communication. 
The  second  form  comprises  the  most  delicate  connecting  fibrillae, 
structures  so  fine  that  their  minute  structure  is  not  understood 
and  we  do  not  know  how  intimate  may  be  the  application  of  the 
fibrillae  to  one  another  or  to  the  surface  of  the  cells.  These  are 
the  typical  plasmodesmen  of  Strasburger  which  he  considers  as 
organs  of  the  plasma  membrane,  kinoplasmic  in  character,  and 
compares  to  cilia.  The  broad  connections  of  the  first  group 
have  exactly  the  structure  that  would  be  expected  of  fused 
pseudopodia,  as  Meyer  pointed  out.  Whether  the  two  types 
insensibly  grade  into  one  another  or  whether  each  is  a  develop- 
ment by  itself  is  a  problem  of  considerable  interest,  for  if  the 
former  possibility  prove  true,  Strasburger's  conception  and  clas- 
sification of  plasmodesmen  as  organs  of  the  cell  will  hardly 
seem  justified. 

When  protoplasmic  connections  become  so  broad  that  cyto- 
plasm flows  or  surges  from  one  cell  'to  another,  an  actual  transfer 
of  nuclei  sometimes  takes  place.  Such  conditions  may  illustrate 
simply  one  extreme  of  the  series  of  protoplasmic  connections 
that  we  have  just  discussed,  but  many  of  them  introduce  some 
complexities,  mainly  through  a  certain  resemblance  to  sexual 
processes,  so  that  they  should  be  treated  apart  from  general 
protoplasmic  connections.  Some  of  them  will  be  described  later 
under  the  head  of  "  Asexual  Cell  Unions  and  Nuclear  Fusions." 

Closely  associated  with  protoplasmic  connections  is  the  inter- 
esting subject  of  intercellular  protoplasm  which  is  receiving 
some  attention  at  present.  The  last  papers  are  by  Kny  (:  04) 
and  Michniewicz  (:  04)  who  are  studying  conditions  in  the  seed, 
especially  of  Lupinus.  By  various  reactions  and  physiological 
studies,  Kny  has  established  an  apparent  identity  of  nature 
between  an  intercellular  substance,  sometimes  with  starch 
inclusions,  and  the  cytoplasm  of  the  neighboring  cells.  He 
considers  this  substance  to  be  intercellular  protoplasm,  that  is, 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  22J 

protoplasm  outside  of  the  cell  walls,  but  connected  with  the 
cytoplasm  within  through  fibrillae.  The  intercellular  proto- 
plasm is  thus  conceived  in  organic  connection  with  nucleated 
cells  and  from  the  studies  of  Townsend  ('97)  we  know  that  non- 
nucleated  protoplasm  may  live  so  long  as  it  is  united  with 
nucleated,  even  though  it  be  by  very  delicate  fibrillae.  Michnie- 
wicz  (:  04)  confirms  Kny's  conclusions  for  Lupinus  and  gives  a 
very  clear  account  of  the  fibrillae  which  connect  the  masses  of 
intercellular  protoplasm  with  neighboring  protoplasts.  These 
studies  make  clearer  a  number  of  observations  of  several  inves- 
tigators (Sauvageau,  Buscalioni,  Schenk,  Magnin,  Strasburger, 
and  others)  who  have  noted  similar  conditions  in  the  tissues 
of  higher  plants  which  are  being  investigated  in  detail  by  Kny. 
Some  of  the  lower  unicellular  forms  likewise  exhibit  an  extra- 
cellular surrounding  film  or  envelope,  which  may  also  be  of  a 
protoplasmic  nature  and  consequently  in  the  same  position  in 
relation  to  the  protoplast  as  intercellular  protoplasm.  Thus  it 
has  been  known  for  many  years  that  the  cells  of  the  Peridinales, 
diatoms,  and  desmids  possessed  extracellular  material,  which 
some  authors  have  considered  in  the  nature  of  slimy  excretions 
but  others  —  Schutt  ('99 ;  :  ooa  ;  :  oob),  Hauptfleisch  ('88  ;  '95), 
Muller  ('98-'99) — have  regarded  as  protoplasmic  in  character. 
Since  the  cell  walls  in  these  forms  are  known  to  possess  pores, 
such  extracellular  substance  must  be  in  close  association  with 
the  cytoplasm  of  the  cell  and  it  is  not  at  all  difficult  to  conceive 
of  it  as  a  part  of  the  protoplasm.  Some  of  the  peculiar  creep- 
ing movements  of  the  diatoms  and  desmids  are  perhaps  expli- 
cable upon  these  facts. 

2.     Sexual  Cell  Unions  and  Nuclear  Fusions. 

The  test  of  a  sexual  act  must  lie  with  the  history  of  the  ele- 
ments which  fuse.  If  these  are  shown  by  their  morphology  and 
developmental  history  to  be  sexual  cells  or  gametes  then  their 
fusion  becomes  a  sexual  process.  There  are  cell  and  even 
nuclear  fusions  which  have  the  physiological  appearances  of 
sexual  acts  but  cannot  be  so  considered  because  the  elements 
concerned  have  plainly  no  relation  to  sexual  cells,  which  are 


228  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

developed  at  other  periods  of  the  life  history,  or  to  the  primitive 
conditions  always  found  with  the  origin  of  sex.  These  exceptional 
processes  will  be  collected  and  described  under  the  heading 
"Asexual  Cell  Unions  and  Nuclear  Fusions,"  following  this 
portion  of  the  paper. 

The  union  of  gametes  is  generally  termed  fertilization.  The 
evolution  of  the  sexual  process  always  tends  towards  a  differ- 
entiation of  the  two  sexual  cells,  one  becoming  more  richly 
stored  with  food  material  and  containing  more  protoplasm  than 
the  other.  This  latter  gamete  is  always  considered  the  female 
and  is  said  to  be  fertilized  when  the  male  gamete,  either  as  a 
motile  sperm  or  reduced  simply  to  a  sperm  nucleus  generally 
with  some  accompanying  protoplasm,  fuses  with  it.  The  most 
evident  morphological  feature  of  fertilization  is  the  close  union 
of  the  gamete  nuclei  so  that  the  chromosomes  of  both  enter  into 
the  mitotic  figure  with  which  the  new  generation  begins. 

We  shall  not  discuss  the  various  forms  of  gametes  nor  their 
habits  in  different  types  of  sexual  reproduction.  They  have 
been  described  in  two  articles  by  the  author  on  the  origin  and 
evolution  of  sex  in  plants  (Davis,  :oi  ;  :  03).  A  detailed  ac- 
count of  the  sexual  reproduction  of  well  known  types  through- 
out the  plant  kingdom  has  been  recently  published  by  Mottier 
(:  O4b)  under  the  title  "  Fecundation  in  Plants  "  a  term  which 
he  prefers  to  fertilization.  This  paper  gives  in  English  the 
most  extensive  summary  of  our  knowledge  of  the  subject  up  to 
the  date  1902  and  will  be  read  with  especial  interest  as  the 
most  available  expression  in  English  of  Strasburger's  general 
views  on  the  significance  of  the  events  connected  with  sexual 
reproduction. 

A  recent  paper  of  Guerin  (:  04)  is  confined  to  an  account  of 
fertilization  in  the  phanerogams  which  are  treated  in  considerable 
detail.  His  discussion  of  double  fertilization  and  parthenogene- 
sis is  of  especial  interest  and  will  be  taken  up  later. 

Our  purpose  is  to  divest  from  the  events  of  sexual  cell  unions 
and  nuclear  fusions  all  secondary  and  unessential  processes  and 
to  outline,  as  are  now  understood,  the  fundamental  phenomena. 
And  to  make  the  subject  more  plain  we  shall  try  to  compare 
in  their  essentials  the  events  of  fertilization  in  plants  with  those 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  229 

in  animals.  Probably  the  most  important  feature  of  fertilization 
is  the  close  union  of  the  gamete  nuclei  through  which  the 
chromosomes  of  both  enter  into  the  first  mitotic  Fgure  of  the 
new  generation.  It  involves  the  organization  of  the  first  cleav- 
age spindle,  which  inaugurates  the  new  generation,  and  the  his- 
tory of  the  paternal  and  maternal  chromosomes  of  the  gametes 
at  this  time  when  the  number  becomes  doubled. 

Several  zoological  papers  have  developed  in  the  past  few  years 
some  very  important  conclusions  concerning  the  individuality  of 
the  paternal  and  maternal  chromosomes,  as  maintained  during 
the  fusion  of  the  gamete  nuclei  and  in  the  formation  of  the  first 
cleavage  spindle.  It  has  been  generally  believed  for  some  time 
—  see  general  review  in  Wilson  (:  oo,  p.  204)  —  that  the  fusion 
of  gamete  nuclei  did  not  involve  a  coalescence  of  the  chromo- 
somes but  that  both  paternal  and  maternal  chromosomes  main- 
tained complete  independence  of  one  another  and  that  all  entered 
into  the  first  cleavage  spindle  as  structures  quite  as  distinct  as 
when  formed  during  spermatogenesis  and  oogenesis.  Hacker 
and  Riickert  have  shown  for  Cyclops  that  the  gamete  nuclei 
divide  side  by  side  in  the  first  mitosis  following  fertilization,  and 
Hacker  followed  these  double  nuclei  as  far  as  the  i6-celled  stage 
when  they  were  still  distinct  from  one  another.  A  few  notable 
investigations  of  recent  years  have  identified  chromosomes  accu- 
rately as  maternal  and  paternal  not  only  in  the  first  cleavage 
spindle  but  through  certain  succeeding  mitoses  and  finally  at 
the  period  of  gametogenesis  when  sperm  and  egg  were  again 
formed.  The  above  principles  have  been  established  chiefly 
through  a  series  of  papers  of  Montgomery,  the  chief  being  a 
lengthy  investigation  of  1901,  and  contributions  of  Sutton 
(:O2;  103)  and  Moenkhaus  (:O4).  They  have  given  us  clear 
evidence  that  the  chromosomes  not  only  maintain  their  com- 
plete individuality  throughout  successive  generations  but  are 
distributed  with  gametogenesis  and  fertilization  in  various  pos- 
sible combinations  that  can  be  expressed  by  mathematical  for- 
mulae furnishing  the  basis  for  certain  ratios  that  approximate 
the  teachings  of  Mendel's  law.  We  shall  have  occasion  to  refer 
to  these  in  Section  V  when  the  subjects  of  gametogenesis,  reduc- 
tion of  chromosomes,  and  hybridization  will  be  discussed. 


230  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

The  same  principles  have  been  established  in  plants  by  recent 
investigations,  some  ot  which  deal  with  oogenesis  and  spermato- 
genesis  and  will  be  specially  treated  in  the  Section  V  while  others 
treat  of  the  behavior  of  the  chromosomes  when  the  gamete  nuclei 
fuse  and  the  sporophyte  generation  begins  its  development.  The 
latter  conditions  concern  the  present  discussion. 

The  history  of  the  chromosomes  in  plants  at  the  time  when 
the  gamete  nuclei  fuse  (fertilization)  is  most  accurately  known 
for  the  pine.  The  last  paper  upon  this  type  (Ferguson,  :  04)  is 
very  complete.  Miss  Ferguson  gives  a  beautiful  series  of  figures, 
some  of  which  we  have  reproduced.  The  sperm  nucleus  comes 
in  contact  with  the  egg  nucleus  and  sinks  into  the  latter  so  that 
it  lies  in  a  depression,  but  as  noted  by  Blackman  ('98),  it  does 
not  penetrate  the  membrane  of  the  egg  nucleus  (Fig.  17,  a). 
Both  gamete  nuclei  thus  lie  side  by  side  occupying  approxi- 
mately the  same  space  formerly  filled  by  the  female.  Each 
shortly  gives  evidence  of  preparation  for  the  mitosis  following 
fertilization  (first  cleavage  spindle).  The  chromatin  of  the  egg 
nucleus  collects  in  a  spirem,  very  close  to  the  sperm,  occupying 
a  relatively  small  portion  of  this  large  female  nucleus  (Fig.  17,  b). 
The  chromatin  of  the  sperm  nucleus  also  takes  position  as  a 
spirem  on  the  side  nearest  its  companion  chromatin  of  the  oppo- 
site sex.  The  remaining  space  of  each  nucleus  is  filled  with  a 
granular  reticulum  of  a  linin  nature.  At  this  time  the  amount 
of  linin  is  extraordinarily  large  in  proportion  to  the  chromatin, 
suggesting  that  some  of  the  latter  substance  has  become  changed 
to  the  former.  Soon,  delicate  fibrillae  appear  around  the  two 
spirems  growing  outward  in  various  directions  and  finally  cross- 
ing from  one  nucleus  to  the  other.  At  the  same  time  the  two 
nuclear  membranes  become  less  distinct  and  shortly  disappear. 
Thus  the  maternal  and  paternal  spirems  come  to  lie  in  a  com- 
mon area  filled  with  delicate  fibrillae  which  run  out  to  the  gran- 
ular cytoplasm  that  lay  around  the  two  gamete  nuclei  (Fig.  17,  c). 
It  should  be  especially  noted  that  at  no  time  in  this  history  has 
there  been  a  resting  nucleus  including  both  maternal  and  pater- 
nal chromosomes  within  a  common  nuclear  membrane.  The 
fusion  of  the  gamete  nuclei  has  only  come  with  the  actual 
formation  of  the  first  cleavage  spindle. 


No.  460.] 


STUDIES   ON  PLANT  CELL.—  V. 


231 


The  fibrillae  organize  a  multipolar  spindle  which  is  very  vari- 
able in  form,  sometimes  with  broad  poles  of  a  multipolar  diarch 
(Fig.  17,  d)  and  at  other  times  almost  as  pointed  as-in-a  typical 
bipolar  spindle  (Fig.  17,  e).  There  are,  of  course,  no  centro- 
somes  and  the  entire  spindle  in  essentially  of  intranuclear  origin. 
The  history  of  its  development  recalls  Miss  Williams'  account 
of  the  spindle  in  the  pollen  mother-cell  of  Passiflora  (Sec.  Ill, 
Amer.  Nat.,  vol.  38,  p.  738,  1904).  During  spindle  formation 
the  spirems  of  the  sperm  and  egg  nuclei  can  be  readily  distin- 
guished as  was  described  by  Blackmail  ('98)  and  Chamberlain 


FIG.  17.  —  Fertilization  in  Pinus  stratus,  a,  conjugating  gamete  nuclei;  b,  the  gamete  nuclei 
still  separated,  with  nuclear  membranes  distinct,  the  maternal  and  paternal  chromatin  in 
two  spirems ;  c,  the  nuclear  membranes  have  disappeared  and  the  two  spirems  lie  close 
together  surrounded  by  the  fibrillse  which  will  organize  the  first  segmentation  spindle;  d, 
prophase  of  the  first  segmentation  spindle,  of  the  multipolar  diarch  type,  paternal  and 
maternal  spirems  still  distinct ;  e,  metaphase  of  first  segmentation  mitosis,  maternal  and 
paternal  chromosomes  now  indistinguishable,  beginning  to  split  in  the  middle  region  (after 
Ferguson,  :o4). 

('99),  but  after  the  two  sets  of  chromosomes  are  formed  (twelve 
of  each)  the  latter  are  brought  so  closely  together  at  metaphase 
of  mitosis  that  the  paternal  and  maternal  cannot  be  separated. 
All  of  the  chromosomes  are  exactly  alike  and  there  is  nothing  in 
the  form  or  size  to  distinguish  one  from  another  as  certain 


232  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

zoologists  have  been  able  to  do  in  some  favorable  animal  types 
(Montgomery,  Sutton,  Moenkhaus).  The  chromosomes  divide 
longitudinally  in  the  usual  way,  the  halves  being  drawn  apart 
from  the  points  of  attachment  of  the  spindle  fibers  (Fig.  17,  e). 
It  is  clear  that  each  daughter  nucleus  receives  a  full  set  of  24 
daughter  chromosomes,  12  of  paternal  and  12  of  maternal 
origin,  and  that  there  is  about  an  equal  amount  of  chromatin 
from  each  sex. 

It  should  be  especially  noted  that  in  the  process  of  fertiliza- 
tion in  the  pine  there  is  at  no  time  present  what  is  generally 
called  a  fusion  nucleus,  /'.  e.,  a  single  nucleus  whose  membrane 
incloses  all  the  material  of  both  male  and  female  gamete  nuclei. 
Such  fusion  nuclei,  as  we  shall  see,  have  been  reported  many 
times  in  other  groups  of  plants  than  the  gymnosperms  where  in 
many  cases,  however,  detailed  studies  are  very  difficult  and  can 
scarcely  be  said  to  have  even  approached  our  knowledge  of  the 
pine. 

Studies  of  other  botanists  indicate  that  the  gymnosperms 
generally  will  show  essentially  the  same  conditions  as  in  the 
pine.  Thus  Woycicki  ('99)  distinguished  in  Larix  two  groups 
of  chromatin  which  he  regarded  as  paternal  and  maternal.  And 
Murrill  (:  oo)  states  for  Tsuga  that  the  chromatin  of  sperm  and 
egg  remain  separate,  forming  two  spirems,  and  only  after  their 
segmentation  into  chromosomes  are  the  two  sets  of  structures 
brought  together  in  the  first  cleavage  spindle.  Land  (:  02) 
figured  the  sperm  nucleus  of  Thuja  imbedded  in  a  depression  of 
the  egg  nucleus.  Miyake  (:  O3a)  noted  that  the  sperm  nucleus 
of  Picea  became  more  or  less  imbedded  in  the  egg  nucleus  while 
the  nuclear  membrane  remained  intact,  and  the  same  author 
(Miyake,  :  O3b),  reports  similar  conditions  in  Abies.  Robert- 
son (:  04)  figures  the  sperm  nucleus  of  Torreya  lying  within  a 
depression  in  the  female  and  with  a  large  amount  of  granular 
cytoplasm  (kinoplasm)  at  the  side.  Coker  ('.03)  states  that 
the  partition  between  the  gamete  nuclei  of  Taxodium  "  does 
not  entirely  disappear  until  immediately  before  the  first  divi- 
sion "  although  the  two  structures  are  closely  united  for  some 
time  previously  while  they  pass  to  the  bottom  of  the  egg. 

Lawson,    studying  Sequoia  (:  O4a)   reports  gamete  nuclei   of 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  233 

about  equal  size  whose  chromatin  contents  unite  in  a  fusion 
nucleus  to  form  a  common  network  in  which  male  and  female 
elements  cannot  be  distinguished.  A  similar  condition  obtains 
in  Cryptomeria,  according  to  Lawson  (:O4b),  where  a  fusion 
nucleus  is  described  in  which  paternal  and  maternal  chromatin 
are  mingled  together  in  a  nucleus  that  passes  through  a  short 
period  of  rest  before  the  development  of  the  first  cleavage 
spindle.  In  view  of  the  work  on  Pinus  I  think  it  may  safely  be 
questioned  whether  in  Sequoia  and  Cryptomeria  the  maternal 
and  paternal  chromatin  really  does  form  a  common  network  in 
the  resting  fusion  nucleus.  The  subject  is  one  very  difficult  of 
study  and  demands  more  stages  than  Lawson  seems  to  have 
followed. 

Fertilization  in  the  cycads  is  not  as  completely  known  as  for 
the  conifers.  Webber  (:oi)  figures  the  sperm  nucleus  of 
Zamia  imbedded  in  the  egg  nucleus  but  quite  distinct  from  it  as 
in  the  pine  but  the  further  history  leading  to  the  development 
of  the  first  segmentation  spindle  was  not  followed.  On  the 
other  hand  Ikeno  ('98b)  described  in  Cycas  the  formation  of  a 
cup-like  depression  in  the  egg  nucleus  to  receive  the  sperm 
nucleus  which  was  said  to  enter  and  fuse  completely  with  the 
female  and  the  same  author  (Ikeno,  :oi)  reports  a  complete 
fusion  of  the  gamete  nuclei  in  Ginkgo  and  did  not  distinguish 
the  paternal  and  maternal  chromosomes  during  the  formation  of 
the  first  segmentation  spindle.  However  it  is  probable  that 
more  detailed  studies  among  the  cycads  and  in  Ginkgo  will 
show  a  behavior  of  the  sperm  nucleus  together  with  the  pater- 
nal and  maternal  chromatin  essentially  similar  to  that  of  the 
conifers.  All  investigations  among  the  cycads  and  in  Ginkgo 
agree  that  cytoplasmic  structures  of  the  sperm  (blepharoplasts, 
cilia,  etc.)  are  left  behind  in  the  cytoplasm  of  the  egg  before  the 
gamete  nuclei  unite. 

Our  knowledge  of  the  details  of  fertilization  in  the  angio- 
sperms  is  surprisingly  meager.  The  only  account  of  the  chro- 
matin is  that  of  Mottier  ('98  ;  :  O4b,  p.  176)  for  Lilium.  He 
describes  and  figures  the  two  gamete  nuclei  as  uniting  with 
their  chromatin  in  the  resting  condition.  The  nuclear  mem- 
branes disappear  at  the  surface  of  contact  and  the  two  nuclei 


234 


THE  AMERICAN  NATURALIST.      [VOL.  XXXIX. 


fuse  into  one.  The  nucleoli  unite  and  so  thoroughly  does  the 
paternal  and  maternal  chromatin  seem  to  be  mixed  in  the  resting 
condition  that  the  fertilized  egg  nucleus  can  scarcely  be  distin- 
guished from  the  unfertilized.  There  would  seem  to  be  then  a 
fusion  nucleus  in  the  lily  with  the  chromatin  in  the  resting 
condition.  The  figures  and  brief  accounts  of  other  botanists 
indicate  that  similar  conditions  may  be  expected  in  other  angio- 
sperms.  But  no  one  has  followed  the  chromatin  in  the  fusion 
nucleus  through  its  later  history,  during  the  organization  of  the 
chromosomes  preparatory  to  the  first  mitosis  following  fertiliza- 
tion. It  would  be  very  surprising  if  paternal  and  maternal 
chromatin  did  not  remain  entirely  independent  of  each  other 
as  in  the  pine.  The  detailed  study  of  fertilization  in  the  angio- 
sperms  presents  a  very  attractive  subject  for  investigation. 
Some  very  interesting  conditions  of  fertilization  have  been 


FIG.  18.  —  Fertilization  in  Ottoclea  sensibilis.  a,  sperm  as  a  spiral  band  within  the  egg  nu- 
cleus ;  b,  later  stage,  the  chromatin  of  the  sperm  much  less  condensed  and  more  widely 
distributed  in  the  egg  nucleus  (after  Shaw,  '983). 

described  in  the  pteridophytes  for  Onoclea  by  Shaw  ('98  a), 
confirmed  by  Mottier  (:  04  a ;  :  04  b),  and  for  Adiantum  and 
Aspidium  by  Thorn  ('99).  In  these  forms  the  male  nucleus 
after  leaving  in  the  protoplasm  of  the  egg  all  of  the  cytoplasmic 
structures  of  the  sperm  (blepharoplasts,  cilia,  etc.)  enters  the 
egg  nucleus  as  a  more  or  less  spiral  body  which  stains  deeply 
and  is  evidently  chiefly  or  wholly  chromatic  in  composition  (Fig. 
1 8).  Within  the  egg  the  dense  structure  of  the  sperm  nucleus 
becomes  looser  by  the  separation  of  the  chromatin  granules  (Fig. 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  235 

1 8,  b)  but  the  form  of  the  sperm  can  be  recognized  for  a  long 
time.  The  chromatin  of  the  egg  nucleus  is  in  a  resting  condi- 
tion at  this  period  and  the  densely  packed  mass- of  paternal 
chromatin  is  very  conspicuous  in  the  loose,  delicate  network  of 
the  female  chromatin.  The  mitosis  following  fertilization  does 
not  occur  for  several  days  so  that  it  is  not  easily  studied  and 
the  organization  of  the  first  cleavage  spindle  with  the  history  of 
the  maternal  and  paternal  chromosomes  has  never  been  followed. 
But  it  is  clear  that  we  have  in  the  pteridophytes  a  true  fusion 
nucleus  containing  for  several  days  both  maternal  and  paternal 
chromatin  within  the  same  nuclear  membrane. 

There  is  only  one  paper  that  gives  any  details  of  fertilization 
in  the  bryophytes,  a  contribution  of  Kruch  ('90)  on  the  liver- 
wort, Riella,  which  seems  to  have  been  generally  overlooked  in 
recent  literature.  After  the  sperm  enters  the  egg,  a  male 
nucleus  is  organized  which  increases  in  size  until  it  is  about 
equal  to  the  egg  nucleus.  The  chromatin  in  both  gamete  nuclei 
is  described  and  figured  as  forming  8  chromosomes  which  are 
organized  before  the  fusion.  The  two  gamete  nuclei  were 
observed,  but  not  figured,  in  contact  and  it  was  not  possible  to 
distinguish  in  size  the  male  from  the  female.  This  account  is 
then  very  different  from  those  of  the  pteridophytes  since  the 
sperm  nucleus  does  not  enter  the  egg  nucleus  but  the  two  fuse 
side  by  side  and  with  their  chromosomes  fully  organized.  There 
are,  however,  some  points  in  Kruch's  paper  that  require  more 
extended  investigation  and  confirmation  in  the  light  of  modern 
research. 

There  is  left  only  the  group  of  the  thallophytes  where  less  is 
known  about  the  detailed  behavior  of  the  chromatin  during  fer- 
tilization than  in  any  region  of  the  plant  kingdom.  The  conju- 
gation of  the  gamete  nuclei  has  been  observed  in  a  number  of 
thallophytes,  representing  all  of  the  higher  groups.  All  of  the 
authors,  with  the  exception  of  Chmielewski  ('90  b)  for  Spirogyra, 
describe  the  product  of  conjugation  as  a  fusion  nucleus,  i.  e., 
one  in  which  the  nuclear  substance  of  both  gametes  is  con- 
tained within  a  common  nuclear  membrane.  The  most  detailed 
accounts  of  the  fusion  of  gamete  nuclei  in  the  thallophytes  are 
those  for  Fucus  (Strasburger,  '97 a;  Farmer  and  Williams,  '98). 


236  THE  AMERICAN  NATURALIST.      [VOL.  XXXIX. 

The  sperm  of  Fucus  upon  entering  the  egg  loses  its  cytoplasm 
and  passes  rapidly  to  the  'egg  nucleus  as  a  deeply  staining  body 
resembling  a  plastid  in  form.  This  structure  is  the  male  nucleus 
whose  chromatin  is  so  densely  crowded  that  it  stains  too  deeply 
to  show  much  structure.  Arriving  at  the  side  of  the  female 
nucleus,  about  ten  minutes  after  its  entrance  into  the  egg,  the 
male  nucleus  flattens  against  the  female  and  increases  in  size  so 
that  the  chromatin  appears  less  condensed.  The  male  nucleus 
is  then  absorbed  so  that  the  paternal  chromatin  lies  within  a 
fusion  nucleus  but  may  be  distinguished  for  some  time  as 
densely  staining  material  at  one  side.  A  second  nucleolus 
often  appears  in  the  fusion  nucleus  in  the  vicinity  of  the  pater- 
nal chromatin  and  is  probably  associated  with  the  entrance  of 
the  sperm  nucleus,  although  it  is  not  likely  to  have  been  brought 
in  as  an  organized  structure  but  developed  later  at  the  expense 
of  material  in  the  sperm  nucleus.  The  fusion  nucleus  remains 
quiescent  for  from  20  to  24  hours  during  which  time  the  paternal 
chromatin  becomes  so  distributed  that  it  can  no  longer  be  fol- 
lowed. Then  two  centrospheres  with  conspicuous  radiations 
appear  at  opposite  poles  of  the  fusion  nucleus  and  the  first 
cleavage  spindle  is  organized.  There  is  no  evidence  that  either 
of  these  centrospheres  is  brought  into  the  egg  by  the  sperm  and 
both  appear  de  novo  and  independently  of  one  another. 

The  chief  accounts  of  the  fusion  of  gamete  nuclei  in  thallo- 
phytes  are  as  follows  :  Closterium  and  Cosmarium  (Klebahn, 
'91);  Rhopalodia  (Klebahn, '96)  ;  Cocconeis  (Karsten,  :oo); 
Sphaeroplea  (Klebahn,  '99 ;  Golenkin,  '99) ;  CEdogonium  (Kle- 
bahn, '92) ;  Coleochseta  (Oltmanns,  '98) ;  Vaucheria  (Oltmanns, 
'95 ;  Davis,  :  04) ;  Fucus  (Strasburger,  '97  a ;  Farmer  and 
Williams,  '98) ;  Batrachospermum  (Schmidle,  '99 ;  Osterhout, 
:oo);  Nemalion  (Wolfe,  104);  Basidiobolus  (Fairchild,  '97); 
Albugo  (Wager,  '96;  Stevens,  '99,  :oib;  Davis,  :oo);  Perono- 
spora  (Wager,  :oo);  Pythium  (Miyake,  :oi  ;  Trow,  :oi);  Ach- 
lya(Trow,  :  04) ;  Araiospora  (King,  :O3);  Sphaerotheca  (Harper, 
'95);  Pyronema  (Harper,  :oo).  Most  of  these  papers  with 
others  on  fertilization  in  the  thallophytes  are  summarized  by 
Mottier,  (:O4b)  in  very  convenient  form  for  reference. 

There  is   some  confusion  in  the  accounts  of  fertilization  in 


No.  460.]  STUDIES   ON  PLANT  CELL—  V.  237 

Spirogyra  which  should  be  thoroughly  investigated.  Chmielew- 
ski  ('90  b)  in  a  paper  published  in  Russian  and  reviewed  in  the 
Bot.  Centralb.,  vol.  50,  p.  264,  1892,  described  a  fusion  of  the 
gamete  nuclei  in  the  zygospore  and  an  immediate  mitosis,  with- 
out a  period  of  rest,  followed  at  once  by  a  second  division  of  the 
daughter  nuclei.  These  mitoses  give  the  zygospore  four  nuclei, 
two  of  which  unite  to  form  a  final  resting  nucleus  in  the  zygo- 
spore while  the  remaining  two  fragment  and  their  products 
finally  break  down.  This  behavior  offers  an  exception  to  all 
sexual  processes  so  far  known  in  the  plant  kingdom.  There  are 
some  features  which  suggest  a  possible  confusion  with  events  as 
described  in  the  zygospore  of  the  desmid  and  the  auxospores  of 
certain  diatoms. 

The  fusion  nucleus  in  the  zygospore  of  Closterium  and  Cos- 
marium  (Klebahn,  '91)  divides  into  four  at  the  time  of  germina- 
tion and  two  of  these  break  down  while  each  of  the  others 
becomes  the  nucleus  of  the  two  new  desmids  that  are  formed. 
There  is  then  in  the  desmids  the  division  of  the  fusion  nucleus 
into  four  but  no  secondary  nuclear  fusions  as  Chmielewski 
reports  for  Spirogyra.  In  certain  diatoms,  Rhopalodia  (Kle- 
bahn, '96)  and  Cocconeis  (Karsten,  :oo),  there  is  a  preliminary 
division  of  the  nuclei  in  each  of  the  two  cells  which  form  the 
auxospore.  In  Rhopalodia  the  mitoses  are  carried  so  far  that 
four  daughter  nuclei  are  formed  in  each  diatom  and  the  pro- 
toplasm divides  into  two  cells  each  of  which  fuses  with  a 
corresponding  cell  of  the  companion  pair.  In  both  types  the 
superfluous  nuclei  break  down  so  that  the  conjugating  cells  have 
each  a  single  functional  gamete  nucleus.  There  are  then  com- 
plications in  the  Conjugales  and  the  diatoms,  which  make  nuclear 
studies  of  the  sexual  processes  exceptionally  difficult  and  we  seem 
justified  in  reserving  our  judgment  of  the  results  of  Chmielewski 
until  confirmed.  It  seems  possible  that  the  mitoses  following  the 
germination  of  the  zygospore  in  the  Conjugales  with  the  attend- 
ant nuclear  degeneration  are  reducing  divisions  in  a  simple  and 
primitive  type  of  sporophyte  generation  but  more  detailed  studies 
of  nuclear  behavior  during  the  formation  and  germination  of  the 
zygospore  will  be  necessary  to  settle  the  discussion. 

We  have  now  finished  our  account  of  nuclear  fusions  in  the 


238  THE  AMERICAN  NATURALIST.        [VOL.  XXXIX. 

sexual  act  (fertilization)  but  there  remains  for  consideration  the 
behavior  of  certain  cytoplasmic  elements  introduced  into  the 
sexually  formed  cell,  especially  chromatophores  and  the  blephar- 
oplast.  Since  the  blepharoplast  bears  a  very  close  resemblance 
to  the  middle  piece  of  the  animal  spermatozoon,  which  some- 
times becomes  a  centrosome  in  the  animal  egg,  a  critical  com- 
parison of  the  behavior  of  these  two  structures  during  fertiliza- 
tion is  full  of  interest. 

Except  for  certain  accounts  of  Spirogyra,  to  be  described  in 
the  next  paragraph,  investigators  agree  that  the  chromatophores 
or  plastids  of  gametes  never  fuse  in  the  sexually  formed  spore. 
Plastids  have  not  been  found  in  the  sperms  of  the  gymnosperms, 
pteridophytes,  nor  bryophytes.  The  sperms  of  some  algae  also 
appear  quite  colorless  at  maturity  but  careful  examinations  have 
shown  in  a  number  of  forms  a  very  small  chromatophore  in  the 
early  stages  of  development.  Other  less  highly  differentiated 
sperms  are  known  to  have  chromatophores  (e.  g.,  Sphaeroplea, 
Cutleria,  Volvox).  Both  gametes  in  the  isogamous  types  of 
sexuality  among  the  algae  always  have  chromatophores  or  plas- 
tids. These  have  been  followed  in  detail  through  stages  of  fer- 
tilization in  Ectocarpus  by  Berthold  (!8i)  and  Oltmanns  ('99), 
and  in  Scytosiphon  by  Kuckuck  ('98)  where  it  is  evident  that 
they  do  not  unite  and  there  is  no  reason  for  believing  that  differ- 
ent conditions  obtain  among  any  of  the  lower  forms  such  as 
Ulothrix,  Cladophora,  Hydrodictyon,  etc.,  although  detailed 
observations  are  greatly  lacking  on  this  point,  chiefly  because 
the  conjugating  cells  are  generally  very  small. 

Early  accounts  of  the  formation  of  the  zygospore  of  Spirogyra 
have  reported  some  form  of  union  of  the  chlorophyll  bands  of 
the  two  gametes.  The  last  work  upon  the  subject,  Chmielewski 
('9oa),  reviews  the  results  of  previous  investigators  and  gives  a 
detailed  account  of  a  species  of  Rynchonema  (Spirogyra). 
Chmielewski  claims  that  the  chromatophore  of  the  gamete  (male) 
that  passes  over  into  the  other  cell  (female)  becomes  disorgan- 
ized as  the  zygospore  develops.  While  the  chlorophyll  band  of 
the  female  cell  retains  much  of  its  color,  that  from  the  male 
becomes  yellowish  and  breaks  up  into  fragments  which  become 
scattered  in  the  zygospore  and  finally  break  down.  This  inter- 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  239 

esting  account  accompanied  by  clear  figures  gives  an  explanation 
far  more  in  keeping  with  what  we  know  and  might  expect  of  the 
behavior  of  chromatophores  in  resting  spores.  That  the  green 
chromatophore  may  temporarily  become  much  modified  in  color 
and  form  is  well  known  in  some  of  the  red  and  orange  resting 
spores  of  the  Volvocaceae  and  the  zygospores  of  the  desmids. 
In  some  of  these  types  the  form  and  color  of  the  chromatophores 
become  quite  lost  for  the  time  being  so  that  studies  on  their 
behavior  are  very  difficult.  For  these  reasons  it  seems  probable 
that  the  accounts  of  the  fusion  of  the  chromatophore  in  the  zygo- 
spore  of  Spirogyra  are  incorrect.  It  is  very  interesting  that  the 
gametes  of  Spirogyra  should  be  so  sharply  differentiated  that  the 
chromatophore  of  one  should  be  reduced  during  conjugation  in 
a  manner  that  resembles  very  closely  the  behavior  of  the  chro- 
matophore in  highly  differentiated  sperms. 

There  is  no  evidence  that  the  pigment  spots,  so  generally 
present  in  the  motile  gametes  of  lower  forms,  ever  unite.  They 
have  been  followed  into  the  zygospore  and  after  the  germination 
of  this  cell  and  they  remain  entirely  independent  of  one  another 
as  would  be  expected  from  their  close  relationships  to  chromato- 
phores. 

The  fate  of  the  blepharoplast  will  now  be  considered.  This 
structure  is  especially  interesting  because  of  its  close  analogy  to 
the  locomotor  apparatus  of  the  animal  spermatozoon,  which  is 
formed  chiefly  from  one  or  more  centrosomes  generally  with  the 
cooperation  of  archoplasm  (idiosome,  Nebenkern).  It  is  also 
claimed  by  a  number  of  zoologists  that  in  some  forms,  at  least, 
the  centrosomes  of  the  first  cleavage  spindle  are  derived  from 
the  spermatozoon. 

All  evidence  indicates  that  the  blepharoplast  of  the  plant 
sperm  is  left  behind  in  the  cytoplasm  of  the  egg  when  the  male 
nucleus  passes  into  the  interior  to  unite  with  the  female  and 
that  centrospheres  when  present,  in  the  first  cleavage  spindle, 
are  formed  de  novo.  The  fate  of  the  blepharoplast  is  clearly 
known  in  Cycas  (Ikeno,  'Q8b),  Zamia  (Webber,  :oi)  and  Ginkgo 
(Ikeno,  :oi).  Soon  after  the  large  top-shaped  sperm  of  these 
forms  enters  the  egg,  the  male  nucleus  slips  out  of  the  spiral 
blepharoplast,  that  partially  invests  it,  and,  leaving  it  with 


240  THE  AMERICAN  NATURALIST.     [VOL.  xxxix. 

other  cytoplasm  of  the  sperm  at  the  end  of  the  egg,  passes 
quickly  to  the  center  to  unite  with  the  female  nucleus.  The 
blepharoplast  remains  near  the  periphery  of  the  egg  and  may  be 
recognized  even  after  the  gamete  nuclei  have  united.  It  finally 
breaks  down  and  its  substance  becomes  lost  in  the  cytoplasm  of 
the  egg.  The  most  complete  account  of  the  history  of  the  ble- 
pharoplast in  the  fertilized  egg  is  that  of  Webber  (  :  o  i ) .  We 
should  naturally  expect  the  first  cleavage  spindle  in  the  cycads 
and  Ginkgo  to  be  developed  as  in  the  conifers.  Ikeno  (:oi) 
described  clearly  an  intranuclear  spindle  in  Ginkgo.  In  the 
conifers,  as  previously  described,  the  first  cleavage  spindle  is 
intranuclear  and  the  fibers  are  developed  freely  from  a  mesh 
and  form  a  broad  poled  spindle  without  centrospheres.  So  that 
not  only  does  the  blepharoplast  break  down  at  a  distance  from 
the  egg  nucleus  but  we  have  no  reason  to  think  that  there  is 
any  place  for  a  centrosome  in  the  history  of  the  first  cleavage 
spindle  in  the  gymnosperms. 

We  do  not  know  clearly  the  fate  of  the  blepharoplast  in  the 
egg  of  any  pteridophyte  or  bryophyte,  although  Shaw's  (*98a) 
studies  on  Onoclea  indicate  that  it  breaks  down  in  the  cyto- 
plasm. Our  knowledge  of  the  thallophytes  is  equally  incom- 
plete as  regards  the  history  of  the  blepharoplast  in  the  egg. 
But  both  Strasburger  ('97a)  and  Farmer  and  Williams  ('98) 
have  agreed  for  Fucus  that  the  two  centrospheres  at  the  poles 
of  the  first  cleavage  spindle  develop  de  novo  and  independently 
of  one  another,  and  Williams  (:  O4b)  holds  the  same  view  for  the 
centrosphere  which  appears  at  the  side  of  the  fertilized  egg  of 
Dictyota.  The  sperms  of  the  thallophytes  are  generally  very 
small  cells  and  it  may  prove  a  difficult  matter  to  follow  their 
blepharoplasts  so  that  our  opinions  of  events  in  these  forms  are 
likely  to  be  largely  inferential  from  our  knowledge  in  higher 
groups. 

We  can  safely  say  that  there  is  no  evidence  that  the  blepharo- 
plast ever  enters  into  the  first  cleavage  spindle  which  is  certainly 
developed  in  the  spermatophytes  and  probably  in  the  pterido- 
phytes  without  centrosomes  or  centrospheres.  Where  centro- 
somes  or  centrospheres  are  known  for  the  first  cleavage  spindle 
in  the  thallophytes  (Fucus  and  Dictyota),  the  observations  indi- 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  241 

cate  that  such  structures  have  not  come  from  the  blepharoplast. 
Williams'  (:  O4b)  recent  work  on  Dictyota,  while  incomplete  in 
the  series  of  stages  illustrating  the  fusion  of  gamete^nuclei  (fer- 
tilization), presents  a  very  interesting  comparison  of  the  devel- 
opment of  the  first  cleavage  spindle  in  fertilized  eggs  with 
parthenogenetic  eggs.  In  the  fertilized  egg  there  is  regularly 
found  a  centrosphere  which  apparently  divides  into  two  that 
separate  until  they  lie  at  opposite  poles  of  the  mature  spindle. 
In  the  parthenogenetic  egg,  on  the  contrary,  the  spindle  is  mul- 
tipolar  and  develops  very  irregularly  from  a  kinoplasmic  mesh 
which  is  intranuclear  and  there  is  no  sign  of  centrospheres. 
Williams  believes  that  fertilization  enables  the  fusion  nucleus 
to  form  de  novo  a  centrosphere  external  to  itself  which  is  not 
possible  for  the  nucleus  of  a  parthenogenetic  egg. 

It  should  be  noted  that  these  conclusions  are  all  against  the 
view  that  the  centrosome  is  a  permanent  organ  of  the  cell  and 
that  the  blepharoplast  holds  any  direct  relation  to  centrosomes 
when  present  in  the  first  cleavage  spindle  and  inferentially  rather 
strengthens  the  doubt  that  the  blepharoplast  is  derived  from  a 
centrosome,  which  point  was  discussed  in  our  account  of  the 
sperm  in  Section  III.  However,  Ikeno  (:O4)  in  a  paper  which 
arrived  too  late  to  be  treated  in  Section  III,  is  very  positive  that 
blepharoplasts  are  centrosomes,  presenting  his  evidence  clearly, 
but  his  explanation  of  the  conditions  under  which  blepharoplasts 
are  formed  from  the  plasma  membrane  does  not  seem  to  me  con- 
clusive, especially  in  the  light  of  Mottier's  (:  O4a)  recent  paper  on 
Chara,  which  also  could  not  be  treated  in  Section  III  (see  Amer. 
Nat.,  vol.  38,  p.  576,  1904). 

3.    Asexual  Cell  Unions  and  Nuclear  Fusions. 

As  stated  earlier  in  the  paper,  the  test  of  a  sexual  act  must 
lie  with  the  history  of  the  elements  which  unite,  unless  we 
choose  to  treat  sexuality  as  a  purely  physiological  process  and 
disregard  its  relation  to  morphology  in  ontogeny  and  phylogeny. 
This  relation  is  so  precise,  i.  e.,  sexuality  is  so  firmly  established 
as  a  fixed  period  in  the  life  history  of  most  organisms,  that  the 
biologist  generally  thinks  of  the  sexual  process  as  a  part  of  the 


242  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

life  history,  which  must  take  place  with  as  much  regularity  as 
the  normal  development  of  any  organ.  As  a  matter  of  fact, 
our  knowledge  of  the  structure  of  sexual  elements  and  the  events 
of  sexual  phenomena  is  almost  wholly  morphological  and  for  the 
present  at  least  it  seems  safer  to  treat  and  define  sexuality  from 
a  morphological  standpoint. 

Under  asexual  cell  unions  and  nuclear  fusions  we  shall  include 
a  number  of  interesting  phenomena  which  can  be  arranged  in 
three  groups :  ( I )  cell  fusions  which  have  apparently  no  sexual 
relations  ;  (2)  cell  fusions  which  are  substitutes  for  a  normal 
ancestral  sexual  process  now  suppressed  ;  and  (3)  extraordinary 
modifications  of  what  may  have  been  originally  sexual  processes 
but  which  at  present  serve  some  peculiar  and  special  function. 

In  the  first  group  will  be  included  the  extensive  union  of 
swarm  spores,  or  the  amoeboid  elements  derived  from  such, 
best  illustrated  in  the  development  of  plasmodia ;  also  such  cell 
fusions  as  are  clearly  for  nutritive  purposes,  as  is  the  union  of 
the  sporophytic  portion  of  the  cystocarp  of  the  red  algae  with 
auxiliary  cells  and  probably  also  the  fusion  of  sporidia  in  the 
smuts  and  the  conjugation  of  yeast  cells.  The  second  group 
embraces  the  interesting  fusions  of  the  nuclei  in  teleutospores 
of  the  smuts  and  rusts  and  in  the  basidium  with  the  previous 
history  of  the  paired  (conjugate)  nuclei  in  the  mycelium,  perhaps 
also  the  nuclear  fusions  in  the  ascus,  and  such  cell  unions  as 
have  been  reported  preliminary  to  the  apogamous  development 
of  the  fern  sporophyte.  The  third  group  includes  the  remarka- 
ble phenomenon  in  the  embryo  sac,  the  double  fusions  of  the 
polar  nuclei  and  the  triple  fusion  of  these  with  the  second  sperm 
nucleus,  frequently  called  "double  fertilization." 

The  well  known  union  of  the  swarm  spores  of  the  Myxomy- 
cetes  as  amoeboid  cells  (myxamcebae)  to  form  the  plasmodium  is 
one  of  the  best  illustrations  of  a  fusion  of  protoplasm  without 
sexual  significance.  In  this  general  union  of  hundreds  and  per- 
haps thousands  of  small  cells  there  are  no  nuclear  fusions  so  far 
as  is  known,  but  simply  the  merging  of  the  cytoplasm  to  form  a 
large  multinucleate  unit.  The  whole  phenomenon  indicates  a 
cooperative  process  which  is  probably  economical  of  nutritive 
functions  in  the  semiterrestrial  conditions  under  which  plas- 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  243 

modia  live.  It  is  quite  possible  that  the  origin  of  sex  may  have 
been  involved  with  some  of  the  same  principles  as  those  which 
bring  about  the  union  of  swarmers  to  form  a  plasrnodium,  but 
the  added  features  of  nuclear  fusion  together  with  the  history 
of  the  sexually  formed  cells  which  become  in  higher  groups  the 
starting  point  of  a  sporophyte  generation  places  the  sexual  act 
on  a  very  much  higher  level  of  complexity. 

There  are  some  records  of  the  union  of  several  zoospores  or 
gametes  to  form  a  zygospore  instead  of  the  usual  conjugation  in 
pairs.  The  biciliate  gametes  of  Acetabularia  (De  Bary  and 
Strasburger,  '77)  sometimes  conjugate  in  threes  and  large 
zygotes  are  figured  with  five  pairs  of  cilia  indicating  that  as 
many  gametes  entered  into  their  formation.  The  gametes  of 
Protosiphon,  described  by  Rostafinski  and  Woronin  ('77)  as  in 
the  life  cycle  of  Botrydium,  are  reported  by  them  to  unite  at 
times  several  together  and  four  are  so  figured.  Klebs  ('96,  p. 
207)  in  his  account  of  Protosiphon  also  noted  the  union  of  the 
gametes  in  threes  especially  when  in  organic  solutions.  The 
significance  of  these  multiple  fusions  of  swarm  spores  is  not 
clear  for  we  know  nothing  of  the  nuclear  history  following  the 
union.  There  is  in  the  habit,  however,  such  a  resemblance  to 
the  extensive  union  of  swarmers  in  the  Myxomycetes  as  to  indi- 
cate that  primarily  sexuality  may  have  been  concerned  chiefly 
with  cytoplasmic  fusions  and  associated  very  intimately  with 
nutritive  processes.  I  have  recently  observed  several  instances 
of  the  conjugation  of  zoospores  of  Saprolegnia  when  the  ele- 
ments united  in  pairs  at  the  ciliated  ends  and  along  the  sides 
exactly  as  do  motile  gametes,  and  the  fused  cell  bore  four  cilia. 
The  zoospores  of  Saprolegnia  are  too  far  removed  morphologi- 
cally from  the  highly  differentiated  sexual  organs  of  the  group 
to  justify  the  explanation  of  such  conjugation  as  a  sexual  act 
and  we  must  think  of  it  as  due  to  some  peculiarities  of  nutritive 
conditions. 

Another  class  of  very  interesting  cell  fusions,  associated  with 
nutritive  functions,  is  presented  in  the  union  of  the  sporophytic 
fertile  filaments  (ooblastema  filaments)  in  the  cystocarp  of  the 
Rhodophyceae  with  auxiliary  cells.  This  phenomenon  which 
was  regarded  by  Schmitz  and  his  followers  as  sexual  in  charac- 


244  THE   AMERICAN   NATURALIST.       [VoL.  XXXIX. 

ter,  is  considered  by  Oltmanns  ('98b)  to  have  nutritive  relations 
alone.  Oltmanns  studied  the  fusion  with  auxiliary  cells  in  sev- 
eral genera,  but  especially  for  Callithamnion  and  Dudresnaya, 
and  is  satisfied  that  the  cell  unions  concern  only  the  cytoplasm. 
Fertilization  takes  place  with  the  fusion  of  gamete  nuclei  in 
the  carpogonia  and  these  cells  develop  the  sporophyte  genera- 
tions. The  fusion  of  fertilized  carpogonia  or  filaments  derived 
from  them  with  auxiliary  cells,  is  a  feature  of  a  sort  of  semipara- 
sitic  relation  that  the  sporophyte  holds  to  the  gametophyte  by 
which  it  is  nourished  in  part  through  organic  connections  with 
the  gametophyte.  The  nuclei  of  the  sporophytic  structures 
remain  quite  apart  from  those  of  the  auxiliary  cells  so  that  the 
union  is  purely  cytoplasmic.  This  theory  of  Oltmanns  has 
received  strong  support  through  the  detailed  nuclear  studies  of 
Wolfe  (:  04)  on  fertilization  and  the  development  of  the  cysto- 
carp  of  Nemalion  who  finds  cytological  evidence  of  the  sporo- 
phytic character  of  the  cystocarp.  These  papers  of  Oltmanns 
and  Wolfe  have  been  discussed  by  myself  in  the  Bot.  Gas.,  vol. 
27,  p.  314,  1899,  and  vol.  39,  p.  64,  1905. 

Writers  have  at  times  attached  sexual  significance  to  the  con- 
spicuous fusions  between  sporidia  of  certain  of  the  Ustilaginales 
(e.  g.,  Tilletia).  But  there  seems  at  present  no  reason  to  regard 
this  phenomenon  as  different  from  the  cytoplasmic  connections 
frequently  established  between  cells  of  hyphae  which  are  ulti- 
mately associated  in  a  common  mycelium  where  the  whole 
forms  a  close  unit  with  respect  to  common  nutritive  relations. 
Such  protoplasmic  connections  were  treated  in  the  first  part  of 
this  section.  Harper  ('99a)  studied  the  union  of  conidia  and 
cells  of  the  promycelium  in  Ustilago  and  concluded  that  the 
fusions  involve  the  cytoplasm  alone,  there  being  no  nuclear 
changes.  However,  Federley  (:  03-:  04  ;  review  in  Bot.  Zeit., 
vol.  62,  p.  171,  1904)  has  observed  the  migration  of  a  nucleus 
from  one  conidium  to  another  in  Ustilago  tragopogonis  pratensis 
(Pers.),  and  a  fusion  within  the  latter.  This  nuclear  fusion  was 
not  found  in  some  other  forms  of  Ustilago  which  behaved  as 
Harper  has  described.  There  is  nothing  in  the  morphology  of 
the  conidia  to  indicate  that  they  are  sexual  cells  and  from  what 
we  know  of  the  life  history  of  Basidiomycetes  we  should  look 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  245 

for  sexual   processes  at  other  periods   more  closely   associated 
with  the  development  of  teleutospores  or  basidia. 

The  conjugation  of  yeast  cells  has  many  points  of  similarity 
to  the  fusion  of  conidia  in  the  Ustilaginales.     This  phenomenon 
has  been  discovered  in  an  organism  obtained  from  commercial 
ginger  by  Barker  (:oi),  which  he  calls  Zygosaccharomyces,  and 
in  three  species  of  Schizosaccharomyces  by  Guilliermond  (:O3). 
The  conjugation  in  all  forms  immediately  precedes  spore  forma- 
tion and  involves  a  nuclear  fusion  as  well  as  that  of  the  cyto- 
plasm.    The  conjugation  is  followed  by  division  of  the  fusion 
nucleus  and  spore    formation    in    the   united   cells.     The    con- 
jugating cells  are  sisters  in  the  species  of  Schizosaccharomyces 
but  apparently  may  not   be   closely   related   in    Barker's  form, 
Zygosaccharomyces.     Both  investigators  regard  the  conjugation 
as  a  sexual  act,  and  Guilliermond  considers  the  fusion  cell  to  be 
an  ascus  with  the  value  of  a  zygospore.     These  conclusions  do 
not  seem  to  the   writer  convincing.      Spore   formation   in  the 
yeasts  has  not  been  shown  to  present  any  of  the  peculiarities  of 
nuclear  division  and  free  cell  formation  as  described  by  Harper 
for  the  ascus,  and  until  such  are  established  it  is  hardly  safe  to 
conclude  that  the  yeasts  are  Ascomycetes.     Whether  or  not  the 
conjugation  is  a  sexual  process  becomes  a  question  of  phylogeny 
and  we  know  too  little  of  the  history  and  relationships  of  the 
yeasts  to  assert  that  the  conjugating  cells  are  morphologically 
gametes.     Again,  the  view  that  yeasts  are  derived  from  conidia 
or  mycelia    of  higher    fungi    which    have    continued   a    simple 
growth   by  budding  in  peculiar  and  favorable   media  is   rather 
against  any  view  that   we  are  dealing  here  with  a  simple  or 
primitive  sexual  act.     There  are  very  striking  resemblances  to 
the  fusions  of  conidia  in  the  Ustilaginales,  which  were  described 
in  the  previous  paragraph  and  do  not  appear  to  be  sexual  proc- 
esses.      It  is  unsafe  to  assume  sexuality  because  the  conjuga- 
tion -precedes   spore   formation,  because  in  most   yeasts   spore 
formation  takes  place  regularly  without  conjugation.     Is  it  not 
rather  another  illustration  of  cell  and  nuclear  fusions  related  to 
nutritive  processes  alone  ? 

Some  of  the    most    interesting    nuclear    fusions,    apparently 
associated  with  the  apogamous  development  of  a  sporophyte  are 


246  THE   AMERICAN  NATURALIS1\       [VOL.  XXXIX. 

the  unions  of  the  pairs  of  nuclei  which  enter  the  cells  of  the 
developing  teleutospores  of  the  Uredinales  and  Ustilaginales 
and  the  basidium  of  higher  Basidiomycetes.  It  has  been  estab- 
lished through  the  studies  of  a  number  of  investigators  (chiefly 
Rosen,  '93  ;  Dangeard  and  Sapin-Trouffy,  '93  ;  Dangeard  '93, 
'94-'95a>  c  I  Poirault  and  Raciborski,  '95  ;  Sapin-Trouffy,  '96  ; 
Maire,  :  oo  a,  b,  c,  :  02  ;  Holden  and  Harper,  :  03)  that  the 
aecidiospores  and  the  mycelium  derived  from  them  and  pre- 
ceding the  development  of  the  uredospores  and  teleutospores 
contain  pairs  of  nuclei  which  divide  in  such  a  manner  (conjugate 
division)  that  the  nuclei  of  the  pair  are  derived  through  two 
unbroken  lines  of  succession  for  a  long  vegetative  period  and 
always  maintain  complete  independence  of  one  another.  Every 
young  teleutospore  and  basidium  contains  such  a  pair  of  nuclei 
which  shortly  fuse  so  that  the  mature  structure  is  uninucleate. 
Dangeard  and  Sapin-Trouffy  have  from  the  first  regarded  the 
nuclear  fusion  within  the  teleutospore,  whether  of  rust  or  smut, 
as  a  sexual  act  and  the  ripe  teleutospore  a  fertilized  egg,  regard- 
less of  the  fact  that  its  morphology  was  not  that  of  any  known 
sexual  organs.  Dangeard  ('94-'95  c  ;  :  oo)  likewise  considered 
the  nuclear  fusions  in  the  basidium  as  sexual.  Raciborski  ('96) 
suggested  that  the  series  of  conjugate  mitoses  leading  to  the 
nuclear  fusions  in  the  teleutospore  represented  a  vegetative 
phase  intercalated  between  the  beginning  of  a  sexual  act  and  its 
finish  in  the  teleutospore.  His  explanation,  in  the  light  of  the 
recent  paper  of  Blackman  (:O4a),  was  nearest  the  truth.  Maire 
(:  02)  presents  the  most  extensive  account  of  the  nuclear  struc- 
ture in  the  higher  Basidiomycetes  previous  to  and  during  the 
formation  of  the  basidia.  He  held  that  the  fusion  of  the  paired 
nuclei  (synkaryon)  in  the  basidium  was  not  the  whole  act  of 
fertilization  which  must  begin  with  the  formation  of  the  paired 
nuclei.  Maire  (:  02,  p.  189)  gave  some  suggestions  as  to  how 
and  where  the  paired  nuclei  arose  but  neither  he  nor  any  of  the 
authors  mentioned  above  knew  clearly  their  origin. 

Blackman  (:  O4a)  has  made  the  most  important  contribution  to 
the  subject  of  fertilization  and  alternation  of  generation  in  the 
Uredinales,  showing  clearly  that  the  paired  nuclei  appear  in  the 
life  history  of  Phragmidium  violaceum  and  Gymnosporangium 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  247 

clavariceforme  just  before  the  development  of  the  aecidium. 
They  arise  in  Phragmidium  by  the  migration  of  a  nucleus  from 
an  adjacent  cell  into  an  element  (the  fertile  cell)  which  represents 
a  female  sexual  organ.  The  morphology  of  the  female  organ  is 
not  clear  but  there  are  suggestions  of  a  structure  similar  to  the 
procarps  of  the  Rhodophyceae  and  Laboulbeniales.  The  fertile 
cell,  after  receiving  its  second  nucleus,  develops  a  chain  of 
aecidiospores,  the  two  nuclei  becoming  so  closely  associated  in 
the  paired  condition  that  they  divide  simultaneously  (conjugate 
mitosis)  from  now  on  until  the  teleutospores  are  formed.  Thus 
the  cells  of  all  mycelium  beginning  with  the  secidiospore  con- 
tain paired  nuclei  up  to  the  development  of  the  teleutospores, 
including  of  course  the  uredospores  when  present.  This  period 
of  the  life  history  may  be  considered  as  representing  a  sporophyte 
generation,  especially  since  the  total  of  chromatin  in  the  pair  of 
nuclei  is  double  the  amount  when  the  nuclei  are  solitary.  The 
sporophyte  phase  ends  with  the  fusion  of  the  pair  of  nuclei  in 
each  cell  of  the  teleutospores  and  in  the  reduction  phenomena 
that  take  place  with  the  germination  of  the  teleutospore,  includ- 
ing the  formation  of  the  promycelium.  The  sporidia  developed 
by  the  promycelium  are  uninucleate  and  the  cells  of  the  mycelium 
derived  from  them  are  uninucleate  up  to  the  production  of  the 
aecidium.  This  constitutes  the  gametophyte  phase  of  the  life 
history.  The  spermogonia  by  their  morphology  seem  to  be 
male  organs,  now  functionless. 

In  such  of  the  Uredinales  as  have  no  aecidium,  as  also  in  the 
higher  Basidiomycetes  and  the  Ustilaginales,  it  is  probable  that 
both  sexual  organs  are  suppressed  since  no  trace  of  such  struc- 
tures has  been  found.  However,  we  may  expect  to  discover 
periods  in  all  of  these  forms  when  paired  nuclei  come  into  the 
life  history  and  after  a  series  of  conjugate  divisions  fuse  in  the 
teleutospore  or  basidium.  Such  pairs  of  nuclei,  as  stated  before, 
are  known  in  the  Ustilaginales  (Dangeard,  '93)  and  in  a  number 
of  forms  of  the  Uredinales  and  the  nuclear  fusions  have  been 
followed  in  the  teleutospore.  H olden  and  Harper  (:  03)  have 
given  an  especially  clear  account  of  the  paired  nuclei  in  the 
mycelium  and  uredospores  of  Coleosporium  together  with  their 
fusion  in  the  teleutospore.  Maire  (:  02)  describes  the  paired 


248  THE   AMERICAN  NATURALIST.       [VoL.  XXXIX. 

t 
nuclei  (synkaryons)  and  their  fusion  in  the  basidium  in  a  large 

number  of  Hymenomycetes  and  Gasteromycetes. 

Evidence  is  thus  accumulating  that  the  cells  in  the  mycelium 
of  higher  Basidiomycetes  (Hymenomycetes  and  Gasteromycetes) 
are  binucleate  for  extended  periods  previous  to  the  formation  of 
basidia  where  nuclear  fusions  always  take  place.  Binucleate  cells 
in  the  higher  Basidiomycetes  were  first  reported  by  Maire  (:  ooa  ; 
:  oob),  in  the  tissue  preliminary  to  spore  formation.  He  also  con- 
firmed Dangeard  ('g^-'g^c)  in  his  view  that  only  two  nuclei  unite 
in  the  basidium  contrary  to  accounts  of  Rosen  ('93)  and  Wager 
('99,  p.  586)  which  described  a  succession  of  fusions  involving 
sometimes  as  many  as  six  or  eight  nuclei.  Harper  (:O2)  has 
given  for  Hypochnus  one  of  the  most  complete  accounts  of  the 
behavior  of  paired  nuclei  previous  to  and  during  the  development 
of  the  basidium.  The  cells  of  the  mycelium  of  this  simple 
Hymenomycete  were  found  to  be  binucleate  as  far  back  as  they 
were  studied  which  included  all  of  the  conspicuous  vegetative 
structure.  Only  a  single  pair  of  nuclei  enters  the  basidium  and 
fuses.  Harper's  results  are  then  in  agreement  with  the  extended 
observations  of  Maire  (:O2)  as  are  also  the  detailed  studies  of 
Ruhland  (:oi)  on  a  number  of  forms  and  Bambeke  (:O3). 
Taken  together  they  seem  to  show  clearly  that  the  mycelium, 
for  long  periods  preliminary  to  the  formation  of  basidia,  contains 
paired  nuclei  and  that  the  basidia  receive  each  a  single  pair, 
which  nuclei  fuse.  There  is  thus  an  exact  correspondence 
between  the  life  histories  of  the  Ustilaginales,  Uredinales,  and 
higher  Basidiomycetes  with  respect  to  the  period  of  paired 
nuclei  and  their  fusion  in  the  teleutospore  or  basidium. 
Dangeard  called  the  fusion  in  the  basidium  a  sexual  act  and  the 
structure  an  oospore  regardless  of  the  morphological  difficulties 
of  such  a  conception.  Maire  (:  02,  p.  202)  states  that  the  origin 
of  the  paired  nuclei  is  the  only  phenomenon  strictly  comparable 
to  fertilization  and  Blackman's  studies  support  this  view.  Ruh- 
land (:oi)  regards  the  conditions  as  a  deviation  from  the  normal 
type  of  sexuality  calling  it  "  intracellular  karyogamy."  The 
origin  of  the  paired  nuclei  is  not  known  for  any  higher  Basidi- 
omycete  and  the  discovery  of  this  period  and  determination  of 
the  events  leading  to  the  change  from  uninucleate  mycelium  to 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  249 

binucleate  is  one  of  the  most  interesting  problems  in  this  field  'of 
botany.  This  is  the  point  where  we  should  expect  to  find  the 
remains  of  sexual  organs,  if  any  are  present  in  _th£  higher 
Basidiomycetes,  but  it  is  not  likely  that  they  will  be  found.  It 
seems  more  probable  that  the  mycelium  with  the  paired  nuclei 
(perhaps  sporophytic  in  character)  arises  apogamously  with  a 
complete  suppression  of  the  sexual  organs  in  agreement  with  such 
of  the  Uredinales  as  have  no  aecidium  and  the  Ustilaginales. 

Blackman's  explanation  of  the  history  of  the  paired  nuclei  in 
Phragmidium  is  full  of  interest.  As  stated  before,  he  regards 
the  fertile  cell  which  develops  a  chain  of  aecidiospores,  "as  a 
female  reproductive  cell  which  undergoes  a  process  of  fertiliza- 
tion by  a  union  with  an  adjacent  cell  of  the  mycelium  and  its 
reception  therefrom  of  a  nucleus.  The  mycelium  then  which 
arises  with  the  aecidiospore  is  sporophytic  in  character  and  so 
remains  until  the  fusion  of  the  pairs  of  nuclei  in  the  teleuto- 
spores.  The  male  organs  of  the  rusts  are  the  spermogonia  and 
the  male  gametes  the  spermatia  which  are  of  course  now  func- 
tionless  so  that  the  "process  of  fertilization"  is  through  the 
introduction  into  the  female  cell  of  a  nucleus  which  is  not  phy- 
logenetically  a  male  sexual  element.  Blackman's  (104 a,  pp. 
349-353;  :O4b)  conception  of  the  process  as  an  act  of  ferti- 
lization involves  some  principles  which  will  be  briefly  outlined. 

Blackman  believes  for  Phragmidium  "  that  the  primitive  normal 
process  of  fertilization  by  means  of  spermatia  has  been  replaced 
by  fertilization  of  the  female  cell  through  the  nucleus  of  an 
ordinary  vegetative  cell  "  and  regards  the  process  as  very  similar 
to  the  phenomenon  reported  in  the  apogamous  development  of 
ferns  by  Farmer,  Moore,  and  Digby  (:  03),  which  will  be  consid- 
ered presently.  Blackman  points  out  that  normal  processes  of 
fertilization  such  as  we  have  included  under  the  head  of  "  sexual 
cell  unions  and  nuclear  fusions  "  do  not  involve  in  many  forms 
(probably  all  types  with  a  sporophyte  generation)  an  immediate 
union  of  the  chromatin  of  the  sexual  nuclei  which  is  known  to 
remain  distinct  during  the  first  cleavage  mitosis  in  a  number  of 
types  (e,  g.,  Pinus  and  some  other  gymnosperms).  So  there  is 
nothing  in  the  delayed  fusion  of  the  paired  nuclei  up  to  the 
teleutospore  that  is  seriously  against  his  explanation  of  the  "fer- 


250  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

tilization "  of  the  female  cell  of  the  Uredinales.  Indeed,  we 
may  expect  to  find  that  the  actual  fusion  of  paternal  and  mater- 
nal chromatin  does  not  take  place  in  the  higher  plants  until  the 
end  of  the  sporophyte  generation  in  the  spore  mother  cell,  as 
zoologists  have  concluded  that  such  union  occurs  just  previous  to 
gametogenesis  in  animals.  But  is  Blackman  justified  in  regard- 
ing the  phenomenon  substituted  for  the  activities  of  ancestral 
sexual  organs  in  Phragmidium,  now  functionless,  as  a  sexual  act 
and  is  it  desirable  to  apply  the  term  fertilization  to  the  phe- 
nomenon ? 

Blackman  (:O4b,  p.  153)  speaks  of  the  introduction  of  a 
nucleus  into  the  fertile  cell  of  the  Uredinales  and  the  phenome- 
non in  the  apogamous  development  of  the  fern  after  the  account 
of  Farmer,  Moore,  and  Digby  (:O3)  as  "  reduced  forms  of  ferti- 
lization." It  may  be  questioned  whether  the  use  of  the  term 
fertilization  is  fully  justified  by  the  events  under  discussion.  We 
are  all  likely  to  agree  with  these  authors  that  the  physiological 
aspects  of  the  phenomena  in  the  cases  under  consideration  are 
similar  to  sexual  acts.  But,  by  the  writer,  the  act  of  fertiliza- 
tion is  always  considered  in  phylogenetic  relations  and  strictly 
limited  to  the  union  of  sexually  differentiated  cells,  which  are 
defined  by  their  morphology  through  principles  of  homology. 
Whenever  on~e  or  both  of  the  gametes  are  suppressed  in  a  life 
history  and  a  succeeding  generation  develops  of  the  sort  that 
normally  follows  a  sexual  act,  then  such  a  development  is  apoga- 
mous and  the  phenomena  always  introduce  features  which  are 
foreign  to  the  processes  of  normal  fertilization  and  the  funda- 
mental principles  of  sexuality. 

Perhaps  the  most  important  characteristic  of  sexuality  from 
an  evolutionary  standpoint  is  the  fusion  of  gametes  of  unrelated 
parentage,  for  in  the  mingling  of  diverse  protoplasm  lie  two 
factors:  (i)  a  physiological  stimulus  to  development,  and  (2)  an 
increased  probability  of  inherited  variation  which  in  new  combi- 
nations will  appear  to  the  advantage  of  the  species.  Blackman's 
"  reduced  forms  of  fertilization"  which  I  should  prefer  to  con- 
sider apart  from  normal  fertilization  as  examples  of  apogamy, 
and  have  so  classed  in  this  treatment,  do  satisfy  the  physiologi- 
cal requirements  of  a  sexual  act  in  that  a  form  of  nuclear  fusion 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  25 1 

is  substituted  for  the  union  of  gamete  nuclei  but  the  phylogenetic 
and  evolutionary  aspects  of  sexuality  are  disregarded.  Also,  the 
nuclei  that  fuse  are  sometimes  very  closely  related,  which  is  a 
condition  generally  avoided  in  sexual  processes  except  where 
peculiarities  of  habit  make  close  inbreeding  necessary.  It  is 
true  that  large  groups,  such  as  the  Basidiomycetes,  perhaps 
certain  regions  of  the  Ascomycetes,  some  Phycomycetes,  and 
some  forms  of  the  higher  plants  and  algae  seem  to  have  given  up 
normal  sexual  processes  but  there  is  much  evidence  that  in  many 
cases  this  loss  of  sexuality  is  associated  with  a  certain  degree  of 
segregation  and  with  peculiarities  of  life  conditions  apart  from 
the  normal  activities  of  all  organisms  or  quite  different  from  the 
ancestral  stock.  The  groups  are  likely  to  be  distinguished  by 
highly  specialized  life  habits  of  a  sort  that  make  it  impossible 
for  inherited  sexual  organs  to  function,  either  through  mechan- 
ical difficulties  or  because  one  or  both  degenerate.  It  seems  to 
me  much  clearer  to  regard  all  illustrations  of  Blackman's 
''reduced  forms  of  fertilization"  under  the  general  term  of 
apogamy  even  though  it  may  be  clear  that  they  are  physio- 
logical substitutes  for  sexual  acts  and  to  reserve  the  term  fertil- 
ization for  the  union  of  gametes  which  can  always  be  clearly 
identified  through  morphology  in  ontogeny  and  phylogeny.  The 
success  of  a  group  even  though  ancestral  sexual  processes  may 
be  suppressed  does  not  enter  into  a  problem  which  is  at  bottom 
a  morphological  one.  Success  is  relative  and  we  really  have  no 
means  of  estimating  its  degree  save  by  actual  experiment.  It  is 
not  likely  that  any  biologist  would  claim  that  sexual  degenera- 
tion is  advantageous  to  any  species  although  the  organic  world 
is  full  of  forms  which  have  dispensed  with  sexuality  and  still 
hold  their  places.  These  are  the  reasons  why  I  have  grouped 
cell  unions  and  nuclear  fusions  as  sexual  and  asexual  on  a  mor- 
phological basis  founded  on  phylogenetic  principles  and  why  in 
Section  V,  we  shall  devote  some  attention  to  the  substitutes  for 
sexuality  under  the  head  of  apogamy. 

The  Ascomycetes  present  a  phenomenon  of  nuclear  fusion 
within  the  ascus  which  may  properly  be  considered  at  this  time 
since  there  is  a  certain  resemblance  to  the  nuclear  fusions  in 
the  teleutospore  and  basidium.  Dangeard  ('94-'95b)  gave  the 


252  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

first  account  of  this  phenomenon  describing  it  for  several  forms. 
The  mother  cell  of  an  ascus  sometimes  terminates  a  hypha  but 
more  commonly  is  situated  a  little  back  from  the  end  at  a  point 
where  the  hypha  bends  abruptly  like  a  knee.  The  mother  cell 
contains  two  nuclei,  closely  related  to  each  other,  that  unite, 
after  which  the  fusion  nucleus  divides  to  form  the  ascospores. 
Dangeard  considered  this  fusion  to  be  a  sexual  act  and  the 
product  an  oospore  which  germinates  immediately  to  form  the 
ascus.  He  regards  the  ascus  as  a  sporangium,  and  equivalent 
to  the  promycelium  which  he  calls  a  conidiophore.  Dangeard 
is  not  willing  to  accept  any  of  the  evidence  that  the  ascocarp 
ever  results  from  a  sexual  act  or  that  sexual  organs  either  func- 
tional or  abortive  are  present  at  any  stage  in  the  life  history  of 
Ascomycetes.  Sexuality,  according  to  him,  is  reduced  to  the 
fusion  within  the  ascus  alone.  He  (Dangeard,  '96— '9/a,  b ; 
:  oo)  discredits  the  work  of  Harper  on  Sphaerotheca,  Erysiphe, 
and  Pyronema  and  the  older  accounts  of  De  Bary  and  his  pupils 
on  sexual  organs  of  the  Ascomycetes.  A  series  of  short  papers 
in  Le  Botaniste  (:  03,  Fas.  i)  presents  Dangeard's  last  attack  on 
the  work  of  Harper  and  a  reafnrmation  of  his  peculiar  views. 

Harper's  description  of  sexual  processes  in  Sphaerotheca  ('95  ; 
'96)  Erysiphe  ('96),  and  Pyronema  (:  oob)  are  so  convincing 
that,  together  with  our  knowledge  of  sexual  organs  in  the 
lichens,  Laboulbeniales,  and  Gymnoascales,  we  must  accept  the 
old  view  of  De  Bary  that  the  ascocarp  represents  a  development 
(probably  sporophytic)  from  a  sexual  phase  even  though  it  may 
be  established  that  there  is  much  apogamy  in  the  Ascomycetes. 
Harper  gives  the  clearest  account  of  the  nuclear  fusion  in  the 
ascus  of  any  author  without,  however,  committing  himself  to 
speculations  on  its  significance.  The  subject  is  well  sum- 
marized in  his  paper  on  Pyronema  (:  oob,  pp.  363,  394).  He 
finds  in  Erysiphe,  Pyronema,  and  some  other  forms  that  the 
ascus  is  always  developed  from  a  penultimate  cell  of  a  hypha 
which  bends  sharply  so  that  this  cell  appears  to  lie  at  the  tip. 
There  are  two  nuclei  at  the  end  of  the  ascogenous  hypha  and 
these  divide  simultaneously  in  a  very  characteristic  manner  so 
that  the  young  ascus  receives  two  of  the  resultant  four  nuclei, 
but  each  is  derived  from  a  different  one  of  the  original  pair  and 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  253 

consequently  they  are  not  sisters.  The  two  nuclei  in  the  ascus 
then  fuse.  The  origin  of  the  original  pair  is  not  known. 

No  satisfactory  explanation  of  this  fusion  in  the  ascus  has 
been  advanced.  The  conditions  in  the  Ascomycetes  are  not  the 
same  as  in  the  Basidiomycetes.  There  is  no  series  of  paired 
nuclei  in  the  ascogenous  hyphse  and  no  evidence  of  a  delayed 
fusion  of  gamete  nuclei  following  a  sexual  act  nor  of  nuclear 
fusions  associated  with  the  apogamous  development  of  a  sporo- 
phyte  generation.  On  the  contrary,  a  sexual  act  with  the 
fusion  of  gamete  nuclei  has  been  clearly  established  in  some 
forms  preliminary  to  the  development  of  the  ascocarp  and  the 
nuclear  union  in  the  ascus  is  plainly  a  supplementary  phenom- 
enon. Wager  and  Harper  point  out  analogies  to  the  account  of 
Chmielewski  ('9Ob)  for  Spirogyra,  considered  in  a  previous  part 
of  this  section,  which  described  a  double  nuclear  fusion  in  the 
zygospore.  Thus  the  primary,  sexually  formed  nucleus  of  the 
zygospore  is  reported  to  divide  into  four  secondary  nuclei,  two 
of  which  break  down  while  the  remaining  two  unite  forming  the 
second  and  final  fusion  nucleus  of  the  spore.  It  is  hard  to  see 
how  these  second  nuclear  fusions  can  be  sexual  and  Groom  ('98) 
is  perhaps  correct  in  considering  them  superimposed  on  the  sex- 
ual act,  but  their  physiological  significance  is  not  clear. 

Some  recent  papers  support  in  general  Harper's  investigations 
on  the  ascus.  Guilliermond  (:  043  ;  :  O4b)  describes  the  devel- 
opment of  the  ascus  and  ascospores  in  a  number  of  forms.  In 
an  unnamed  species  of  Peziza  he  found,  however,  that  the  ascus 
developed  from  the  terminal  cell  of  the  ascogenous  hypha  which 
received  two  nuclei  (that  fuse)  of  the  four  that  are  found  at  the 
tip.  Maire  (:  O3a ;  :  O3b)  has  reported  a  similar  history  for 
Galactinia  succosa.  Both  Maire  and  Guilliermond  note  the 
resemblance  of  these  conditions  to  the  nuclear  associations  in 
the  young  basidium  and  Maire  does  not  hesitate  to  consider  the 
two  nuclei  in  the  tip  of  the  ascogenous  hypha  as  much  reduced 
synkaryons,  (paired  nuclei)  appearing  for  a  very  short  period 
just  previous  to  the  nuclear  fusions  in  the  ascus.  Maire  fol- 
lows Dangeard  in  denying  the  sexual  processes  described  by 
Harper  in  the  Ascomycetes  and  would  allign  the  events  in  the 
ascus  with  those  in  the  basidium.  Guilliermond  agrees  with 


254  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

Harper  that  the  number  of  chromosomes  presented  in  the 
mitoses  within  the  ascus  is  large  (8,  12,  16,  in  various  species) 
as  against  Dangeard  and  Maire  who  have  claimed  that  the 
number  is  uniformly  4.  Guilliermond's  account  of  spore  forma- 
tion in  the  ascus  supports  that  of  Harper  (described  in  Section 
II)  in  all  essentials  and  gives  especial  attention  to  the  structure 
of  the  epiplasm  and  its  inclusions. 

In  summary :  the  significance  of  the  nuclear  fusions  in  the 
ascus  seems  very  much  of  a  mystery.  If  they  could  be  associ- 
ated with  an  apogamous  development  of  the  ascocarp  we  should 
have  conditions  analogous  to  those  in  the  Basidiomycetes  but 
following  a  sexual  act  as  it  does  in  Sphaerotheca,  Erysiphe,  and 
Pyronema  we  find  a  phenomenon  whose  raison  d'  etre  is  not 
apparent.  However,  we  do  not  know  the  history  of  the  nuclei 
preceding  the  group  of  four  at  the  end  of  the  ascogenous  hypha 
and  perhaps  it  may  be  discovered  that  events  at  this  period  are 
concerned  with  nuclear  reduction  at  the  end  of  a  sporophyte 
generation. 

One  of  the  most  interesting  announcements  of  recent  months 
is  that  in  a  preliminary  note  of  Farmer,  Moore,  and  Digby  (:  03) 
on  the  nuclear  history  preceding  the  apogamous  development  of 
a  species  of  Nephrodium.  They  found  that  the  cells  of  the 
prothallus  at  the  point  where  the  sporophyte  arose  became 
binucleate  by  the  migration  of  nuclei  from  neighboring  cells. 
The  two  nuclei  might  remain  separate  for  some  time  or  fuse  at 
once.  The  authors  speak  of  the  whole  process  "as  a  kind  of 
irregular  fertilization"  and  Blackman  considers  it  analogous  to 
the  entrance  of  the  nucleus  into  the  fertile  cell  of  Phragmidium 
and  the  establishment  of  the  paired  nuclei  in  the  Uredinales. 
As  we  discussed  the  phenomenon  in  that  connection  I  consid- 
ered the  use  of  the  term  fertilization  unfortunate  since  it 
included  processes  which  however  similar  physiologically  held  no 
relation  morphologically  and  phylogenetically  to  normal  sexual 
processes.  As  stated  then,  it  seems  to  me  much  clearer  to 
regard  all  such  apogamous  phenomena  apart  from  sexual  proc- 
esses, pointing  out  as  far  as  possible  physiological  resemblances 
but  recognizing  the  wide  gap  in  morphology  established  by  the 
past  evolutionary  history  of  the  plant.  The  interest  in  the  phe- 


No.  460.]  STUDIES   ON  PLANT  CELL V.  255 

nomena  does  not  become  less  by  this  treatment  which  certainly 
avoids  much  confusion  of  expression. 

There  is  left  for  consideration  one  other  group_ol  nuclear 
fusions  which  may  have  sexual  significance  although  such  is 
not  obvious,  namely  the  fusions  of  polar  nuclei  in  the  embryo 
sac  of  angiosperms  and  the  triple  unions  of  the  above  with  a 
second  sperm  nucleus  which  is  often  called  "double  fertiliza- 
tion." Several  excellent  reviews  of  this  subject  have  appeared, 
notably  by  Strasburger  (:  oob),  Sargant  (:  oo),  Coulter  and 
Chamberlain  (:  03),  Mottier  (:O4a,  b),  and  Guerin  (:O4).  The 
explanation  of  this  phenomenon  is  likely  to  rest  finally  upon 
morphological  analysis  but  at  present  we  are  uncertain  of  the 
homologies  of  the  polar  nuclei  and  the  part  they  play  in  the 
evolutionary  history  of  the  endosperm.  The  most  striking 
theory  of  the  endosperm  was  proposed  by  LeMonnier  ('87)  who 
suggested  that  the  fusion  of  the  polar  nuclei  gave  origin  to  a 
second  embryo  modified  to  nourish  the  normal  embryo.  One 
of  the  polar  nuclei  is  always  closely  related  to  the  egg  nucleus 
so  that  in  the  triple  fusions  (the  sperm  with  two  polar  nuclei) 
we  have  conditions  very  close  to  normal  fertilization,  the  dis- 
cordant element  being  not  the  sperm  nucleus  but  the  antipodal 
polar  nucleus.  The  triple  fusions  would  seem  at  first  thought 
to  be  rather  favorable  to  LeMonnier's  theory  although  it  is  plain 
that  with  such  a  diverse  mixture  of  chromatin  from  thre.e  nuclei 
the  resultant  structure  can  scarcely  be  called  a  sporophyte 
embryo  from  the  very  grotesqueness  of  its  make-up.  Miss 
Sargant  considers  the  fusion  of  the  second  sperm  with  the 
micropylar  nucleus  as  sexual  in  character  but  so  complicated 
by  the  introduction  of  the  antipodal  polar  nucleus  that  the 
result  is  a  bizarre  structure  not  strictly  comparable  to  a  normal 
embryo.  In  the  final  solution  of  this  problem  we  must  know 
whether  in  phylogeny  the  sperm  and  micropylar  polar  nucleus 
fused  first  and  the  antipodal  entered  into  the  process  later  or 
whether  the  polar  nuclei  began  the  habit  and  the  second  sperm 
nucleus  was  drawn  afterwards  into  the  activities.  Should  the 
first  possibility  be  established  the  sexual  nature  of  the  process 
would  seem  clear  while  in  the  second  the  events  would  be  of 
the  nature  of  asexual  nuclear  fusions.  While  we  know  very  little 


256  THE  AMERICAN  NATURALIST.         [VOL.  XXXIX. 

of  the  origin  and    evolution  of  the  endosperm  in  angiosperms 
there  is  some  evidence  in  favor  of  the  second  possibility. 

Strasburger  (:  oob)  holds  that  the  double  and  triple  nuclear 
fusions  in  the  embryo  sac  are  not  true  sexual  acts  even  though 
they  may  involve  an  important  principle  of  fertilization,  namely, 
a  stimulus  to  growth.  According  to  him,  sexual  processes  pre- 
sent two  distinct  features  which  he  designates  as  "  generative 
fertilization"  and  "  vegetative  fertilization."  Generative  fertili- 
zation deals  with  the  mingling  of  ancestral  hereditary  substances 
in  the  nuclei  and  establishes  the  basis  for  such  characters  as 
hold  the  species  true  to  its  past  or  introduce  new  qualities  as 
variations  into  the  germ  plasm.  Vegetative  fertilization  brings 
to  the  fusion  nucleus  simply  a  stimulus  to  growth  such  as  may 
be  given  to  unfertilized  eggs  by  changes  in  their  physical  and 
chemical  environment.  We  might  apply  this  classification  to 
many  of  the  examples  of  asexual  nuclear  fusions  which  we  have 
discussed,  as  in  the  apogamous  development  of  the  fern  and  the 
origin  of  the  paired  nuclei  in  the  rusts,  and  they  have  the  ele- 
ments of  vegetative  fertilization  in  Strasburger's  sense.  But 
such  distinctions  are  very  subtle  and  it  seems  rather  doubtful 
whether  they  add  much  to  the  clearness  of  our  conceptions. 
The  growth  stimulus  of  "  vegetative  fertilization "  is  always 
an  accompaniment  of  ''generative  fertilization"  and  would  be 
expected  of  any  cell  unions  or  nuclear  fusions.  The  pecul- 
iarities of  sex  lie  in  the  phylogenetic  features  of  the  phenomena, 
/.  e.,  in  the  union  of  differentiated  gametes  with  their  long  evolu- 
tionary history  and  not  in  the  mere  fusion  of  any  nuclei  at  any 
time. 

From  this  point  of  view  the  double  fusions  of  polar  nuclei  or 
the  triple  fusions,  when  a  sperm  nucleus  becomes  involved  in 
the  phenomenon,  are  of  very  doubtful  sexual  nature  since  no 
phylogenetic  connections  have  been  established  with  the  normal 
sexual  processes  of  the  spermatophytes.  Indeed,  there  are  many 
irregularities  in  the  process  of  endosperm  formation  which  com- 
plicate the  discussion  and  make  it  very  difficult  to  trace  relation- 
ships. Thus  nuclear  fusions  are  described  in  the  late  stages  of 
endosperm  formation  when  several  of  the  free  nuclei  become 
included  in  the  same  cell  area  by  the  formation  of  the  cell  walls 


No.  460.]  STUDIES   ON  PLANT  CELL.— V,  257 

(Corydalis,  Strasburger,  '80  ;  Tischler,  :  oo  ;  Canna,  Humphrey, 
'96).  Such  nuclei  are  known  to  unite  two  or  more  and  some- 
times several  together  within  the  cells,  forming  fusion  nuclei 
with  a  large  and  variable  number  of  chromosomes.  In  Peperomia 
and  Gunnera  the  endosperm  nucleus  results  from  the  fusion  of 
several  free  nuclei  and  a  number  of  instances  are  recorded  in 
which  no  fusion  of  the  polar  nuclei  takes  place,  but  the  endo- 
sperm is  derived  from  the  division  of  one  or  both.  Such  irregu- 
larities, which  will  probably  be  greatly  increased  in  number  as 
investigations  proceed,  indicate  that  the  double  and  triple 
fusions  preceding  the  differentiation  of  the  endosperm  nucleus 
are  not  of  phylogenetic  importance  but  are  more  likely  to  be 
special  developments  in  relation  to  peculiarities  of  seed  forma- 
tion among  the  angiosperms  rather  than  of  a  sexual  nature. 

However,  the  triple  fusions,  when  a  sperm  enters  into  the 
composition  of  the  endosperm  nucleus,  seem  to  furnish  a 
cytological  explanation  of  the  phenomenon  of  xenia  and  thus 
come  into  very  close  physiological  relations  to  sexual  processes. 
In  xenia  we  find  the  effects  of  hybridization  expressed  immedi- 
ately outside  of  the  embryo  in  the  endosperm  of  the  seeds.  If 
paternal  chromatin  has  entered  into  the  composition  of  the  endo- 
sperm nucleus  or  should  the  sperm  nucleus  by  itself  give  rise  to 
a  series  of  endosperm  nuclei  the  appearance  of  paternal  char- 
acters would  be  expected.  This  explanation  of  xenia  was  worked 
out  independently  by  DeVries,  Correns,  and  Webber,  the  last 
author  having  published  a  particularly  clear  and  full  account  of 
the  phenomenon  (Webber,  :oo).  Even  though  the  relation  of 
xenia  to  hybridization  is  apparent,  it  is  nevertheless  clear  that 
we  are  dealing  with  an  exceptional  process  only  possible  because 
of  the  unusual  conditions  within  the  embryo  sac  which  allow  a 
second  sperm  nucleus  to  enter  into  the  activities  of  seed  forma- 
tion and  it  is  certainly  not  established  that  these  activities  have 
any  phylogenetic  relations  to  past  sexual  processes. 

Some  interesting  studies  of  Nemec  (:  02-:  03  ;  :  04)  upon 
asexual  nuclear  fusions  may  open  the  way  for  explanations  of 
some  of  the  examples  which  we  have  considered  as  asexual  in 
the  latter  portion  of  this  paper.  Nemec  found  that  mitosis  in 
the  root  tip  of  Pisum  sativum  could  be  checked  during  anaphase 


258  THE  AMERICAN  NATURALIST.       [VoL.  XXXIX. 

by  treating  the  material  with  chloral  hydrate  so  that  no  walls 
were  formed  between  the  daughter  nuclei,  which  remained  in 
the  common  mother  cell  and  presently  fused  with  one  another. 
The  fusion  nucleus  presented  a^  double  number  of  chromosomes 
(twice  that  of  the  normal  sporophyte)  in  succeeding  mitoses 
which  became  reduced  in  a  few  hours  so  that  later  divisions 
showed  the  number  characteristic  of  the  sporophyte.  Nemec 
regards  nuclear  fusions  and  reduction  phenomena  as  self  regulat- 
ing processes  which  follow  the  vital  cell  fusions  characteristic  of 
fertilization.  The  latter  (cell  fusions)  are  then  the  essential 
phenomena  of  sex  and  nuclear  activities  follow  automatically. 
Reduction  phenomena  are  atavistic  in  character.  Nemec  con- 
siders these  results  in  serious  conflict  with  Strasburger's  ('94) 
theory  of  the  periodic  reduction  of  the  chromosomes,  believing 
that  the  number  of  chromosomes  is  not  so  likely  to  give  the 
characters  of  the  respective  sporophyte  and  gametophyte  gener- 
ations as  other  factors. 

Nemec's  contribution  is  chiefly  of  interest  to  us  in  the  present 
connection  as  showing  that  nuclear  fusions  may  result  from  dis- 
turbances of  the  normal  environment  very  far  removed  from  the 
conditions  that  produce  sexual  cells.  And  this  emphasizes  our 
contention  that  sexual  processes  must  be  judged  through  phylo- 
genetic  analysis  and  not  by  physiological  resemblances.  Thus 
the  nuclear  fusions  in  the  ascus,  in  the  basidium,  preceding  apog- 
amous  development  of  the  fern,  and  perhaps  the  union  of  polar 
nuclei  in  the  embryo  sac  may  be  involved  with  special  physio- 
logical conditions  although  they  resemble  outwardly  sexual 
processes  and  are  sometimes  a  substitute  for  these.  But  never- 
theless they  are  asexual  nuclear  fusions  lacking  that  funda- 
mental character  of  sexuality,  the  result  of  sexual  evolution, 
namely,  a  fixed  position  in  a  life  cycle  established  by  phylogeny 
and  expressed  by  the  classic  phrase  "  ontogeny  repeats  phylog- 
eny." They  are  departures  from  the  normal  life  history  either 
apogamous  in  character  or  concerned  with  some  other  peculiarity 
of  the  plants'  existence. 


No.  460.]  STUDIES   ON  PLANT  CELL.—  V.  259 


LITERATURE   CITED  IN   SECTION  IV,   "THE   PLANT  CELL." 

BAMBEKE. 

:  03.     Sur   1'evolution    nucle*aire    et    la    sporulation    chez  Hydnangium 
carneum  Wallr.      Mem.  d.  1'Acad.  Roy.  Sci.,  Litt.,  Beaux  Arts  d. 
Belgique,  vol.  54. 
BARKER. 

:  01.     A  Conjugating  Yeast.     Phil.  Trans.  Roy.  Soc.  London,  vol.  194, 

p.  467. 
BERTHOLD. 

'81.     Die  geschlechtliche  Fortpflanzung  der  eigentlichen   Phaeospo  reen 

Mitt.  a.  d.  Zool.  Sta.  Neapel,  vol.  2,  p.  401. 
BLACKMAN. 

'98.     The  Cytological  Features  of  Fertilization  and  related  Phenomena  in 
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268  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

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vol.  58,  p.  39,  1900. 


VOL.  XXXIX,  No.  463  JULY, 

THE 

AMERICAN 
NATURALIST 


A   MONTHLY   JOURNAL 

DEVOTED  TO  THE  NATURAL  SCIENCES 
IN    THEIR    WIDEST   SENSE 


CONTENTS 

Page 

I.   Eestoration  of  the  Titanothere  Megacerops     .       PROFESSOR  R.  8.  LULL      419 
II.    Synopses  of  North  American  Invertebrates.    XXI.    The  Nemerteans. 

Part  I PROFESSOR  W.  R.  COE      425 

III.  Studies  on  the  Plant  Cell. -VI DR.  B.  M.  DAVIS      449 

IV.  Notes  and  Literature:  Zoology,  McMurrich's  Human  Embryology,   The 

Arthropods  and  Coelenterates  of  the  Maldive  and  Laccadive  Archipel- 
agoes, Townsend's  Birds  of  Essex  County,  Massachusetts,  Notes     .       .       501 
V-    Correspondence  :  A  Biological  Station  in  Greenland,  Fleas  and  Disease      .       505 


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WILLIAM  S.  BAYLEY,  PH.D.,  Colby  University,  Waterville. 
DOUGLAS  H.  CAMPBELL,  PH.D.,  Stanford  University. 
J.  H.  COMSTOCK,  S.B.,-  Cornell  University,  Ithaca. 
WILLIAM   M.  DAVIS,  M.E.,  Harvard  University,  Cambridge. 
ALES  HRDLICKA,  M.D.,   U.S.  National  Museum,  Washington. 
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ARNOLD  E.  ORTMANN,  PH.D.,   Carnegie  Museum,  Pittsburg. 
D.  P.  PENHALLOW,D.Sc.,F.R.M.S.,  Me  Gill  University,  Montreal. 
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ISRAEL  C.  RUSSELL,  LL.D.,  University  of  Michigan,  Ann  Arbor. 
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STUDIES    ON    THE   PLANT    CELL.  — VI. 

BRADLEY   MOORE  DAVIS. 

SECTION  V.     CELL  ACTIVITIES  AT  CRITICAL  PERIODS  OF 
ONTOGENY  IN  PLANTS. 

WE  shall  discuss  in  this  paper  the  behavior  of  the  protoplasm 
at  a  number  of  critical  periods  in  the  life  history  of  plants  when 
the  organism  passes  from  one  phase  to  another  of  a  fundamen- 
tally different  character.  At  such  times  great  changes  take 
place  in  the  potentialities  of  the  cells  which  inaugurate  the  new 
developments,  changes  that  are  generally  most  conspicuously 
shown  in  the  structure  of  the  nucleus.  Some  of  the  most  inter- 
esting events  of  cell  and  nuclear  history  take  place  at  these 
times,  as  would  be  expected  from  the  importance  of  the  phe- 
nomena. We  shall  treat  the  material  under  the  following  heads  : 
(i)  Gametogenesis,  (2)  Fertilization,  (3)  Sporogenesis,  (4)  Re- 
duction of  the  Chromosomes,  (5)  Apogamy,  (6)  Apospory,  (7) 
Hybridization,  (8)  Xenia. 

i .    GAMETOGENESIS. 

The  events  of  gametogenesis  are  clearly  known  for  the  higher 
plants  but  there  is  some  confusion  and  almost  no  detailed  infor- 
mation in  the  accounts  of  the  thallophytes  where  the  nuclei  are 
very  small  and  the  details  of  the  mitoses  preceding  the  forma- 
tion of  sexual  cells  exceedingly  difficult  of  study. 

There  is  complete  agreement  among  all  investigators  that  the 
mitoses  which  precede  the  differentiation  of  gamete  riuclei  in 
spermatophytes,  pteridophytes,  and  bryophytes  are  typical  karyo- 
kinetic  figures  not  differing  essentially  in  the  behavior  of  the 
chromosomes  from  the  mitoses  generally  characteristic  of  the 
gametophyte  generation.  This  information  is  based  upon  a 


450  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

large  number  of  studies  of  nuclear  figures  in  antheridia  and 
archegonia,  the  generative  cell  of  the  pollen  tube  and  micropylar 
region  of  the  embryo-sac.  There  are  no  reduction  phenomena 
in  these  higher  groups  at  the  period  of  gametogenesis. 

The  subject  is  complicated  in  some  types  of  spermatophytes 
where  the  gametophyte  phase  is  so  reduced  that  the  mitoses 
which  precede  gametogenesis  may  follow  immediately  upon  the 
two  mitoses  characteristic  of  sporogenesis  or  be  separated  from 
them  by  only  one  or  two  divisions.  For  example,  it  is  known 
in  several  types  of  the  lily  family  (Lilium,  Tulipa,  Fritillaria, 
Erythronium,  etc.)  that  the  two  mitoses  of  sporogenesis  (hetero- 
typic  and  homotypic)  are  included  in  the  embryo-sac  and  become 
a  part  of  that  gametophyte  history.  The  third  and  final  mitosis 
in  this  history  differentiates  the  egg  in  the  micropylar  end  of 
the  embryo-sac  and  is  a  typical  nuclear  division.  This  subject 
was  treated  in  some  detail  in  Section  III  of  these  "Studies" 
(Amzr.  Nat.,  vol.  38,  pp.  741-745,  1904).  When  the  mitoses  of 
sporogenesis  are  not  included  within  the  embryo-sac  we  find 
almost  without  exception  three  typical  mitoses  preceding  the 
differentiation  of  the  egg  in  the  angiosperms  and  a  very  large 
number  in  the  gymnosperms,  and  of  course  in  the  pteridophytes 
and  bryophytes  the  whole  vegetative  period  of  the  gametophyte 
which  is  generally  green  and  self-supporting.  There  are  from 
two  to  three  mitoses  in  the  pollen  grain  and  male  gametophyte 
of  the  angiosperms  before  the  development  of  the  sperm  nuclei 
and  a  somewhat  larger  and  more  variable  number  among  the 
gymnosperms.  It  is  necessary  at  the  outset  to  understand 
clearly  what  are  the  events  of  gametogenesis  in  spermatophytes 
because  several  authors  have  carried  the  phenomena  of  sporo- 
genesis over  into  the  period  of  gametogenesis,  where  it  can 
have  no  proper  place  in  exact  morphology.  Such  papers  will 
be  treated  in  connection  with  "  Sporogenesis  "  and  "  Reduction 
of  the  Chromosomes,"  for  they  concern  primarily  these  phe- 
nomena alone. 

Gametogenesis  must  be  considered  at  present  chiefly  from 
our  knowledge  of  the  conditions  in  the  higher  plants  as  they 
furnish  almost  the  only  detailed  information  that  we  have  on 
the  subject.  Upon  this  as  a  basis  we  are  justified  in  suggesting 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  45 1 

possibilities  in  the  thallophytes  which  must  remain  as  specula- 
tions until  investigations  have  advanced  much  farther  in  this 
difficult  field  of  cell  study.  The  basis  of  any  theories  at  present 
must  be  phylogenetic,  a  principle  that  has  not  been  followed  in 
some  of  the  work  upon  the  thallophytes. 

Gametogenesis  in  plants  is  full  of  interest  because  of  the 
sharp  differences  from  the  processes  of  spermatogenesis  and 
oogenesis  in  animals.  In  animals  the  period  of  gametogenesis 
is  one  of  unusual  activity.  After  the  germ  cells  are  differenti- 
ated there  follows  a  period  of  cell  growth,  with  the  peculiar 
activity  termed  synapsis,  during  which  the  number  of  chromo- 
somes is  reduced  to  one  half  the  number  characteristic  of  the 
species.  The  germ  cells  emerge  from  the  growth  periods  as 
primary  spermatocytes  or  oocytes  which  give  rise  respectively 
by  two  successive  mitoses  to  four  spermatids  or  to  an  egg  with 
its  accompanying  polar  bodies.  The  gametes  have  one  half  the 
number  of  chromosomes  characteristic  of  the  species,  so  that 
the  period  of  gametogenesis  is  one  of  chromosome  reduction. 
The  character  of  this  process  of  reduction  will  be  considered 
when  we  take  up  the  analogous  phenomena  in  plants  after  the 
discussion  of  sporogenesis.  Gametogenesis  in  plants  is  in  strik- 
ing contrast  to  that  in  animals.  In  all  higher  groups  (those 
above  the  thallophytes)  we  know  that  the  gametes  have  the 
same  number  of  chromosomes  as  the  vegetative  cells  of  the 
parent  plant  (gametophyte).  There  is  no  reduction  of  the  chro- 
mosomes at  the  time  of  gametogenesis,  that  phenomenon  taking 
place  at  the  end  of  the  sporophyte  generation  with  sporogenesis. 
Also,  there  are  no  peculiarities  of  the  mitoses  immediately 
preceding  gametogenesis  excepting  such  as  concern  the  devel- 
opment of  cilia-bearing  organs  (blepharoplasts)  or  slight  pecul- 
iarities in  the  form  or  size  of  the  spindles,  for  such  nuclear 
figures  are  frequently  different  in  these  particulars  from  the 
mitoses  in  vegetative  cells  of  the  gametophyte.  The  differences 
concern  chiefly  the  structure  of  the  sperm,  and  have  been  de- 
scribed in  our  account  of  that  structure  (Amer.  Nat.,  vol.  38, 
July  and  August,  p.  576,  1904). 

To  Strasburger  above  all  others  should  be  given  the  credit 
of  making  clear  these  important  characteristics  of  gametogene- 


452  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

sis  in  plants.  Strasburger's  paper  of  1894  on  "  The  Periodic 
Reduction  of  the  Number  of  Chromosomes  in  the  Life  His- 
tory of  Living  Organisms"  (Annals  of  Bot.,  vol.  8,  p.  281)  was 
the  first  elaborate  presentation  of  the  principles  of  gametogene- 
sis  and  reduction  phenomena  in  plants  and  has  become  classical 
as  the  foundation  of  the  present  attitude  in  botanical  science 
and  the  basis  and  stimulus  of  a  large  amount  of  confirmatory 
research.  The  matter  really  crystallized  after  the  discovery  that 
the  sporophyte  generation  of  the  higher  plants  possessed  nuclei 
with  twice  the  number  of  chromosomes  characteristic  of  the 
gametophyte  and  that  the  reduction  took  place  in  the  spore 
mother-cell  just  previous  to  sporogenesis. 

These  facts  were  gradually  established  by  a  number  of  investi- 
gations beginning  with  Strasburger  ('84,  '88)  and  Guignard  ('84, 
'85).  Guignard  ('91)  presented  the  first  complete  count  of  the 
number  of  chromosomes  in  the  life  history  of  a  plant  (Li/inm 
martagoii),  determining  the  reduction  period  to  be  in  the  spore 
mother-cell,  and  Overton  ('93  a  and  b)  independently  reached 
the  same  conclusions  for  the  same  plant  and  extended  the  knowl- 
edge of  the  chromosome  count  in  gametophyte  and  sporophyte 
to  a  number  of  other  types.  Overton 's  paper  was  important  in 
its  suggestiveness  for  extended  research  among  the  higher  cryp- 
togams. Other  investigations  followed  shortly  in  the  gymno- 
sperms,  pteridophytes,  and  liverworts,  all  supporting  the  view 
that  the  nuclei  of  the  sporophyte  generation,  following  the  fusion 
of  gamete  nuclei*  had  double  the  number  of  chromosomes  char- 
acteristic of  the  gametophyte  and  that  the  reduction  phenomena 
occurred  at  the  end  of  the  sporophyte  generation  in  the  spore 
mother-cell.  The  significance  of  reduction  phenomena  at  sporo- 
genesis must  be  phylogenetic  since  it  represents  a  return  of  the 
organism  at  this  time  to  the  ancestral  gametophyte  condition. 
The  details  of  this  literature  belong  to  the  account  of  "  Sporo- 
genesis "  and  "  Reduction  of  the  Chromosomes,"  and  will  be 
taken  up  later.  But  it  is  necessary  to  present  the  outline  at 
this  time  to  make  clear  the  important  fact  that  no  reduction  of 
the  chromosomes  takes  place  during  gametogenesis  in  all  groups 
above  the  thallophytes. 

The  theories  of    gametogenesis  among  the  thallophytes   rest 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  453 

upon  information  which  in  point  of  completeness  falls  very  far 
short  of  our  knowledge  of  the  groups  above.  Indeed,  no  forms 
have  been  studied  with  the  detail  that  is  known  in  higher  groups 
chiefly  for  the  reason  that  the  investigator  is  forced  to  deal  with 
very  small  nuclei  and  mitotic  figures  whose  chromosomes  are 
exceedingly  minute  and  because  of  various  technical  difficulties. 
The  theories  in  general  fall  into  two  groups  :  (i)  those  which 
have  an  obvious  basis  in  attempts  to  reconcile  events  with  the 
processes  of  gametogenesis  in  animals,  and  (2)  those  proceeding 
from  the  view  that  for  phylogenetic  reasons  the  periods  and  phe- 
nomena of  gametogenesis  in  the  lower  plants  should  correspond 
with  those  of  the  higher. 

We  may  pass  over  with  a  few  words  the  early  crude  attempts 
to  establish  structures  for  plants  comparable  to  the  polar  bodies 
of  animals.  For  example  at  the  conclusion  of  oogenesis  in  some 
algae  (e.  g.,  Vaucheria,  CEdogonium)  a  globule  of  slime  is  exuded 
with  the  opening  of  the  oogonium.  It  was  suggested  that  such 
material  is  thrown  off  from  the  egg  but  we  now  know  that  it  is 
not  protoplasmic  in  character  but  is  apparently  derived  from  a 
softening  of  the  cell  wall.  Then  the  ventral  canal  cell  has  been 
compared  to  a  polar  body  but  it  seems  clear  now  that  all  of 
the  canal  cells  are  homologous  and  a  part  of  what  was  form- 
erly an  extensive  gametogenous  tissue  within  the  archegonium. 
Then  the  small  group  of  cells  cut  off  below  the  oogonium  of  the 
Charales  and  the  fragmented  nuclear  material  in  the  trichogyne 
of  the  red  algae  have  been  compared  to  substance  thrown  off 
from  the  egg  but  without  any  knowledge  of  the  nuclear  struc- 
ture. Finally  the  nuclear  degeneration  which  is  a  very  conspic- 
uous feature  of  oogenesis  in  certain  groups  whose  oogonia  are 
multinucleate  (Peronosporales,  Saprolegniales,  Pelvetia,  etc.) 
has  been  considered  related  to  reduction  phenomena.  But  the 
nuclei  in  all  of  these  forms  bear  every  evidence  of  being  in  each 
type  homologous  structures  whose  large  numbers  have  a  phylo- 
genetic raison  d'etre  and  the  extensive  degeneration  is  associated 
with  the  principles  of  sexual  evolution  which  tend  to  conserve 
protoplasm  for  the  good  of  a  lesser  number  of  gamete  nuclei 
even  to  the  sacrifice  of  others  that  are  potentially  equivalent. 

We  will  now  consider  the  few  instances  among  the  thallo- 


454  THE  A  At  ERIC  AN  NATURALIST.       [Vou  XXXIX. 

phytes  in  which  a  reduction  of  the  chromosomes  is  reported  just 
previous  to  or  during  gametogenesis.  The  best  known  case  is 
Fucus  since  this  type  has  been  studied  by  three  investigators : 
Farmer  and  Williams  ('98)  and  Strasburger  ('97a).  They  agree 
in  describing  the  nuclear  figure  that  differentiates  the  oogonium 
from  the  stalk  cell  as  exhibiting  a  large  number  of  chromosomes 
(28  or  30)  while  the  three  mitoses  within  the  oogonium,  which 
give  rise  to  the  eight  eggs,  present  only  one  half  that  number 
(14  or  15).  Apparently  there  is  a  reduction  by  one  half  just 
before  the  mitoses  in  the  oogonium.  Since  there  is  no  sporo- 
phyte  generation  in  Fucus  it  is  of  course  difficult  to  compare 
these  conditions  with  those  in  higher  plants,  but,  as  will  be 
explained  later,  there  are  some  reasons  why  we  should  not 
expect  to  find  reduction  phenomena  at  gametogenesis  in  any 
thallophyte. 

Reduction  phenomena  at  gametogenesis  have  also  been  sug- 
gested for  various  types  of  the  Peronosporales  and  Saproleg- 
niales  but  not,  however,  in  exactly  the  same  way  as  in  Fucus. 
There  are  always,  as  far  as  is  known,  one  or  two  mitoses  within 
the  oogonium  before  the  gamete  nuclei  are  organized  and  it  has 
been  held  that  these  are  reduction  divisions  by  Rosenberg  for  the 
Peronosporales  and  by  Trow  for  the  Saprolegniales.  Rosenberg 
(:  O3b)  described  for  the  oogonium  of  Plasmopara  a  condition  of 
synapsis  in  the  nuclei  preceding  the  two  mitoses  and  compared 
this  sequence  with  the  events  of  sporogenesis  in  higher  plants 
in  which  the  two  divisions  within  the  spore  mother-cell  are  pre- 
ceded by  a  period  of  synapsis.  Rosenberg  did  not  determine  the 
number  of  chromosomes  in  the  vegetative  nuclei  so  that  he  has 
no  positive  evidence  of  reduction  in  the  oogonia.  With  respect 
to  the  two  mitoses  and  the  preliminary  synapsis  I  have  already 
pointed  out  in  criticism  of  Rosenberg's  studies  (Bot.  Gaz.,  vol. 
36,  p.  154,  1903)  that  the  number  of  mitoses  is  variable  in  the 
oogonia  of  the  Peronosporales  and  Saprolegniales  and  apparently 
entirely  absent  in  the  species  of  Vaucheria  studied  by  myself 
(Davis,  :O4a).  Also,  the  phenomenon  of  synapsis,  which  is 
easily  recognized  in  the  large  nuclei  of  the  spore  mother-cell, 
would  be  difficult  to  establish  in  the  small  nuclei  within  the 
oogonia  of  the  forms  mentioned  above.  Nuclei  can  be  found 


No.  463.]  STUDIES   ON  PLANT  CELL.— VI.  455 

in  a  number  of  structures  with  their  contents  somewhat  massed 
at  one  side  or  in  the  center  but  such  conditions  must  not  be 
confused  with  the  remarkable  process  of  synapsis  Jn_the  spore 
mother-cell.  Among  all  the  excellent  studies  of  gametogenesis 
in  the  Peronosporales  I  cannot  find  any  clear  evidence  of  a  re- 
duction of  the  chromosomes  at  gametogenesis. 

Quite  different  is  the  account  that  Trow  (104)  brings  forward 
to  support  his  view  of  chromosome  reduction  during  gametogen- 
esis in  the  Saprolegniales.  Trow  describes  two  mitoses  in  the 
oogonium  of  Achlya  debaryana :  in  the  first  the  number  of  chro- 
mosomes is  eight  which  becomes  reduced  to  four  in  the  second. 
Trow's  account  of  a  second  mitosis  in  Achlya  is  very  different 
in  a  number  of  particulars  from  the  results  of  all  investigations 
on  gametogenesis  in  the  Peronosporales  and  Saprolegniales. 
Two  centrosomes  with  radiations  are  said  to  appear  at  the  poles 
of  the  spindle  at  anaphase,  structures  which  were  not  present  in 
the  first  mitosis.  Some  of  these  asters  become  the  center  of 
the  egg  origins  and  are  later  accompanied  by  deeply  staining 
material  constituting  a  body  which  Trow  terms  an  ovocentrum 
and  which  perhaps  corresponds  to  a  coenocentrum.  Relatively 
few  of  the  nuclei  in  the  oogonium  are  said  to  pass  through  this 
second  mitosis  and  some  of  their  products,  with  the  accom- 
panying asters,  break  down.  The  remainder  become  the  func- 
tional gamete  nuclei  of  the  eggs.  There  are  many  complex 
activities  described  by  Trow  in  connection  with  the  appearance 
of  the  asters  during  the  second  mitosis  and  also  at  the  side  of 
the  sperm  nuclei  which  are  said  to  enter  the  oogonium,  events 
that  cannot  be  correlated  with  the  processes  of  gametogenesis 
and  fertilization  as  we  understand  them  for  the  Peronosporales. 
They  are  treated  briefly  in  a  review  by  myself  (Bot.  Gas.,  vol. 
39,  p.  6 1,  1905),  where,  however,  I  misunderstood  a  distinction 
that  Trow  draws  between  the  aster  and  the  ovocentrum  (see  an 
answer  by  Trow,  Bot.  Gaz.,  vol.  39,  p.  300,  1905).  My  impres- 
sion is  that  either  Trow  has  been  mistaken  in  his  interpretations 
or  that  there  are  present  events  which  must  entirely  change  our 
conception  of  gametogenesis  in  the  Saprolegniales  and  Perono- 
sporales, but  which  are  not  fully  explained  by  Trow's  paper. 

Let  us  now  think  of  gametogenesis  among  the  thallophytes 


456  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

with  reference  to  what  we  know  of  the  process  in  higher  groups 
and  the  principles  of  the  origin  and  evolution  of  sex  and  the 
sporophyte  among  the  lower.  It  seems  clear  that  the  sporo- 
phyte  generation  is  characterized  by  a  double  number  of  chromo- 
somes as  a  result  of  the  fusion  of  gamete  nuclei  at  fertilization. 
We  must  then  lay  the  fundamental  inception  or  origin  of  the 
sporophyte  to  the  stimulus  of  the  sexual  act.  That  is,  the  sexu- 
ally formed  fusion  cell  must  have  different  potentialities  from 
the  germ  plasm  of  the  parent  gametophyte  and  it  cannot  pro- 
duce a  gametophyte  again  until  these  potentialities  are  worked 
off  and  the  protoplasm  returns  to  the  dead  level  of  the  ancestral 
stock  (the  gametophyte).  By  the  potentialities  of  the  sporo- 
phyte plasm  we  mean  primarily  a  greater  energy  or  growth 
stimulus  which  must  express  itself  differently  from  the  gameto- 
phyte. Morphologically  we  can  only  distinguish  sporophyte 
plasm  from  gametophyte  plasm  by  the  double  number  of  the 
chromosomes  but  of  course  the  complexities  of  the  sexual  act 
would  make  great  differences  in  the  chemical  structure  of  the 
t\vo.  The  divergences  in  the  history  of  the  gametophyte  and 
sporophyte,  as  shown  throughout  ontogeny  and  phylogeny,  are 
but  the  final  expressions  of  the  different  potentialities  of  the 
protoplasm  in  each  generation.  The -morphological  forms  of 
expression  of  the  sporophyte  are  extraordinarily  various  and  in 
the  long  evolutionary  history  of  this  generation  have  developed 
great  structural  differentiation  but  with  every  life  history  the 
sporophyte  has  the  same  beginning  (fertilization,  with  the  doub- 
ling of  the  chromosomes)  and  the  same  ending  (sporogenesis, 
with  chromosome  reduction).  Between  the  beginning  and  the 
end  is  intercalated  a  vegetative  period,  short  and  simple  in  some 
forms,  and  very  long  and  elaborate  in  others.  The  history  of 
the  development  of  this  vegetative  period  or  the  evolution  of 
the  sporophyte  is  a  subject  far  outside  of  and  secondary 
to  the  scope  of  this  discussion.  We  are  only  concerned  with 
the  protoplasmic  activities  at  the  beginning  (fertilization)  and 
the  end  (sporogenesis)  of  the  sporophyte  generation. 

We  know  nothing  of  the  behavior  of  the  chromosomes  in 
types  of  the  thallophytes  which  illustrate  most  closely  our  con- 
ception of  the  origin  of  sex  and  of  the  sporophyte  generation. 


OF  THE 

UNIVERSITY 


No.  463.]  STUDIES  ON  PLANT  CELL.— VI.  457 

I  refer  to  many  lower  algae  such  as  Ulothrix,  forms  of  the 
Volvocaceas,  CEdogonium,  Coleochaete,  and  many  others.  How- 
ever, the  homologies  of  primitive  gametes  and  their  origin  from 
types  of  asexual  zoospores  is  very  clear  in  a  number  of  groups. 
We  can  see  nothing  in  the  morphology  and  mode  of  develop- 
ment of  these  reproductive  cells  to  suggest  reduction  phenomena 
when  gametes  are  produced.  The  primitive  gamete  is  generally 
somewhat  smaller  than  its  homologue  the  zoospore,  often  because 
the  protoplasm  of  the  gamete  mother-cell  becomes  distributed  in 
a  greater  number  of  daughter  elements.  It  is  well  known  that 
the  conditions  that  lead  to  conjugation  are  exceedingly  variable, 
depending  upon  environmental  factors  and  one  often  cannot  tell 
at  the  time  whether  a  swarm  spore  will  show  sexual  habits  or 
germinate  without  conjugation.  The  most  satisfactory  theory 
of  the  origin  of  sex  in  plants  regards  primitive  gametes  as 
weaker  or  lacking  in  certain  potentialities  of  vegetative  growth 
and  the  conjugation  as  a  mutually  cooperative  process  resulting 
in  a  rejuvenescence  of  the  protoplasm.  The  fact  that  many 
simple  types  of  gametes  will  germinate  without  fertilization  and 
produce  small  and  weak  sporelings  shows  that  vegetative  possi- 
bilities are  not  entirely  lost.  Investigations  on  the  chromosome 
history  among  these  forms,  difficult  though  they  be,  are  some  of 
the  most  interesting  subjects  of  botanical  research.  We  know 
some  general  principles  of  the  origin  and  evolution  of  sex  in 
plants  (Davis,  :oib,  :  O3a)  but  of  the  chromosome  history  in  the 
simplest  types  of  gametogenesis  nothing  is  known. 

With  respect  to  the  history  of  the  chromosomes  in  the  sim- 
plest sporophytes  we  are  also  as  ignorant  as  in  the  simplest 
types  of  gametogenesis.  We  have  excellent  reasons  for  believ- 
ing that  the  sporophyte  generation  is  represented  among  the 
thallophytes  in  a  number  of  very  simple  conditions.  Numbers 
of  zygospores  and  oospores  (c.  g.,  Ulothrix,  CEdogonium,  forms 
of  the  Conjugales  and  Volvocaceas,  etc.)  give  rise  on  germination 
to  several  daughter  cells.  In  higher  forms  this  growth  period  is 
lengthened  to  the  formation  of  a  reproductive  tissue  (Coleochaete) 
and  in  the  great  groups  of  the  Rhodophyceae,  Ascomycetes,  and 
Basidiomycetes  there  is  present  an  extensive  development  from 
the  fertilized  female  cell  (or  its  equivalent  when  apogamy  obtains) 


458  THE  AMERICAN  NATURALIST.      [VOL.  XXXIX. 

involving  the  development  of  a  vegetative  structure  before  the 
period  of  sporogenesis.  From  the  studies  of  Wolfe  (:  04)  we 
know  that  the  sporophyte  portion  of  Nemalion  (the  cystocarp) 
contains  nuclei  with  double  the  number  of  chromosomes  (about 
1 6)  present  in  the  gametophyte  (about  8)  and  that  the  period  of 
chromosome  reduction  is  apparently  just  previous  to  the  devel- 
opment of  the  carpospores  (sporogenesis).  Williams  (:O4a  and 
b)  has  recently  determined  that  the  asexual  plant  of  Dictyota  is 
a  sporophyte  generation  with  double  the  number  of  chromosomes 
(32)  found  in  the  sexual  plant  (16).  The  reduction  occurs  here 
during  a  rather  long  period  of  preparation  on  the  part  of  the 
nucleus  in  the  tetraspore  mother-cell  and  the  reduced  number 
appears  in  the  two  mitoses  that  form  the  tetraspores.  These 
events  closely  parallel  those  in  the  spore  mother-cell  of  higher 
plants  and  will  be  discussed  further  under  "  Sporogenesis." 

William's  (:  O4b)  account  of  gametogenesis  in  Dictyota  is  the 
most  complete  that  we  have  for  any  thallophyte.  The  oogonia 
and  antheridia  are  cut  off  from  a  stalk  cell  by  a  mitosis  which 
presents  16  chromosomes,  the  number  characteristic  of  the 
gametophyte.  The  contents  of  the  oogonium  forms  a  single 
egg  and  consequently  presents  no  mitotrc  phenomena.  The 
antheridium  develops  over  1500  sperms  thus  exhibiting  a  large 
number  of  successive  divisions.  These  all  show  16  chromosomes 
and  the  mitoses  are  typical,  not  differing  in  any  essential  from 
the  division  in  the  stalk  cell.  The  entire  absence  of  mitoses  in 
the  oogonium  and  the  great  number  in  the  antheridium  are 
striking  facts  which  show  that  no  especial  significance  can  be 
attached  to  nuclear  divisions  within  sexual  organs  of  this  type. 
There  is  no  place  for  reduction  phenomena  within  these  sexual 
organs  and  none  precede  their  development. 

These  studies  of  Williams  and  Wolfe  justify  us  in  expecting 
that  other  thallophytes  will  support  their  discoveries  that  the 
product  of  the  sexual  act  will  have  a  fusion  nucleus  with  double 
the  number  of  chromosomes  present  in  the  sexual  plant  (game- 
tophyte) and  that  reduction  phenomena  may  be  expected  to  fol- 
low the  sexual  act  and  not  precede  it  as  in  animals.  In  such 
thallophytes  as  have  no  sporophyte  generation  we  may  suppose, 
as  Strasburger  ('94a)  suggested,  that  the  number  of  chromo- 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  459 

somes  is  reduced  with  the  germination  of  the  sexually  formed 
cell  so  that  the  protoplasm  returns  at  once  to  the  potentialities 
of  the  gametophyte.  It  is  quite  possible  that  the_four  zoo- 
spores  produced  from  the  oospore  of  CEdogonium  and  the  four 
nuclei  found  in  the  germinating  zygospores  of  the  desmids  and 
Spirogyra  may  indicate  divisions  concerned  with  reduction 
phenomena  similar  to  those  in  the  tetraspore  mother-cells  of 
Dictyota  (which  may  also  be  expected  in  the  tetraspore  mother- 
cell  of  the  red  algae)  and  in  the  spore  mother-cell  of  the  higher 
plants. 

For  these  reasons  we  seem  to  be  justified  in  taking  a  critical 
attitude  towards  the  accounts  of  chromosome  reduction  at  game- 
togenesis  among  the  thallophytes.  The  logic  of  the  situation 
would  lead  us  to  expect  that  every  sexual  act  gives  a  doubling 
of  the  chromosomes  and  an  impulse  towards  the  development 
of  a  sporophyte  phase  in  plants  which  must  be  worked  off  before 
the  protoplasm  is  in  condition  to  reproduce  the  parent  gameto- 
phyte. Reduction  phenomena  should  follow  then  every  sexual 
act.  If  it  takes  place  immediately  with  the  germination  of  the 
sexually  formed  cell  there  is  of  course  no  sporophyte  generation. 
Because  the  conception  of  the  sporophyte  generation  with  reduc- 
tion of  the  chromosomes  at  sporogenesis  is  so  clearly  established 
in  higher  groups,  those  investigators  who  claim  reduction  phe- 
nomena at  gametogenesis  must  expect  their  views  to  be  severely 
scrutinized  and  accept  the  responsibility  of  presenting  very  clear 
and  convincing  proof  of  their  conclusions.  The  author  does 
not  think  that  this  evidence  is  supplied  in  satisfactory  form  by 
any  investigation  so  far. 

2.  FERTILIZATION. 

In  Section  IV  of  these  "  Studies  "  we  described  the  most 
important  phenomena  of  fertilization  under  the  caption  "  Sexual 
Cell  Unions  and  Nuclear  Fusions."  It  will  not  be  necessary  to 
discuss  the  facts  of  the  phenomena  in  detail  again.  This  account 
will  take  up  the  more  theoretical  aspects  of  the  events  of  ferti- 
lization and  their  relation  to  other  critical  periods  of  ontogeny. 

Plants  are  in  complete  agreement  with  animals  in  the  follow- 


460  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

ing  chief  events  and  principles  of  fertilization.  Thus  Van 
Beneden's  conclusion  of  1883  that  sexual  nuclei  are  equivalent 
in  their  chromatin  content  at  the  time  of  fusion  irrespective  of 
differences  in  size  is  admirably  borne  out  by  Miss  Ferguson's 
(:  04)  studies  on  the  pine.  In  this  form  as  in  the  gymnosperms 
generally  the  male  nucleus  is  much  smaller  than  the  female  and 
comes  to  lie  in  a  depression  in  the  latter  before  the  actual  fusion 
takes  place.  After  the  fusion  the  paternal  and  maternal  chromo- 
somes are  found  in  two  groups  side  by  side  preparatory  to  the 
first  cleavage  mitosis  and  are  indistinguishable  except  for  their 
position  ;  the  chromatin  of  the  two  sexes  is  equal  in  amount  as 
far  as  can  be  seen.  Then  the  observations  of  the  Hertwig 
brothers,  in  1887,  and  Boveri,  in  1889  and  1895,  that  the  sperm 
nucleus  could  enter  and  cause  the  development  of  denucleated 
eggs  or  their  fragments  thus  taking  the  part  of  a  female  nucleus 
in  parthenogenesis,  were  established  for  plants  by  Winkler's 
(:oi)  experiments  on  Cystoseira.  Winkler  was  able  to  divide 
the  egg  of  this  brown  alga  into  a  nucleated  and  a  non-nucleated 
portion  and  he  found  that  sperms  entered  the  non-nucleated 
parts  and  caused  them  to  develop  sporelings  side  by  side  with  the 
fertilized  nucleated  portions.  The  sporelings  from  the  non-nucle- 
ated fragments,  controlled  by  the  sperm  nuclei  alone,  developed 
about  half  as  rapidly  as  those  from  the  originally  nucleated  por- 
tions which  of  course  were  dominated  by  sexually  formed  fusion 
nuclei,  but  the  two  sets  of  sporelings  were  alike  in  form  as  far  as 
they  were  grown.  Only  with  respect  to  Boveri's  celebrated 
theory  that  the  sperm  brings  to  the  egg  in  the  centrosome  the 
mechanism  of  cell  division,  do  plants  fail  to  support  the  conclu- 
sions of  certain  zoologists  with  respect  to  the  most  important 
events  of  fertilization.  This  point  upon  which  zoologists  are 
not  in  full  accord  will  be  discussed  later.  There  is  general 
agreement  in  the  view  that  the  male  nucleus  of  plants  supplies 
chromosomes  equal  in  number  and  equivalent  quantitatively  to 
the  female,  and  general  accord  in  the  conclusions  that  the  chro- 
mosomes by  their  individuality,  apparent  permanence  of  struc- 
ture, and  fixed  behavior  must  be  bearers  of  hereditary  characters. 
Evidence  from  the  most  recent  investigations  upon  favorable 
forms  of  both  animals  and  plants  indicates  that  the  chromosomes 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  461 

from  both  gametes  maintain  their  independence  and  never  fuse 
at  the  immediate  time  of  fertilization.  We  have  reason  to 
assume,  chiefly  from  zoological  studies,  that -the_patern.al  and 
maternal  chromosomes  of  plants  remain  independent  throughout 
the  entire  sporophyte  generation  and  that  no  fusion  takes  place 
until  the  period  of  chromosome  reduction  at  sporogenesis.  If 
no  sporophyte  generation  is  present  we  should  expect  the  fusion 
and  reduction  of  the  chromosomes  to  occur  after  the  sexually 
formed  cell  had  passed  through  a  period  of  rest  (for  all  reduction 
phenomena  seem  to  require  considerable  time)  unless  there  be 
actually  such  reduction  during  gametogenesis  in  the  thallophytes 
as  reported  for  Fucus  and  Saprolegnia.  The  morphology  of  the 
chromosomes  is  probably  unchanged  by  the  immediate  act  of 
fertilization.  The  fusion  nucleus  simply  contains  double  the 
number  of  chromosomes  present  in  each  gamete  nucleus  which 
increases  by  so  much  the  metabolic  possibilities  which  lie  in 
these  structures. 

Besides  chromatin  the  sperm  brings  into  the  egg  a  certain 
amount  of  cytoplasm.  Some  of  this  may  be  the  substance  of 
the  blepharoplast  or  other  kinoplasm  associated  with  the  nucleus 
but  there  is  often  besides  considerable  granular  trophoplasm, 
sometimes  with  inclusions  of  starch  and  other  food  substances, 
and  the  male  gamete  of  certain  thallophytes  contains  a  chroma- 
tophore.  There  is  no  reason  to  suppose  that  development 
especially  characteristic  of  fertilization,  the  sporophyte  genera- 
tion, has  any  relation  to  this  trophoplasm  with  its  food  inclusions, 
excepting  as  it  may  stimulate  growth  which  is  to  be  expected 
whenever  organic  food  material  is  introduced  into  protoplasm. 
But  we  can  hardly  believe  that  the  formative  elements  or  the 
rudiments  of  further  development  especially  those  of  a  sporo- 
phytic  character  lie  in  this  region  of  the  protoplasm.  They 
must  be  sought  in  the  nuclei  and  in  the  only  stable  elements  of 
the  nuclei,  the  chromosomes. 

It  has  been  held  at  times  by  botanists,  following  the  lead  of 
certain  zoologists,  that  the  sperm  or  sperm  nucleus  introduced  a 
centrosome  into  the  egg  which  organized  the  first  cleavage- 
spindle  and  thereby  played  a  necessary  part  in  starting  cell 
division.  Such  a  centrosome  would  naturally  be  sought  in  the 


462  THE  AMERICAN  NATURALIST.       [VOL.  XXX IX. 

blepharoplast  which  is  clearly  analogous  to  the  middle  piece  of 
the  animal  spermatozoon.  We  have  no  evidence  that  such  events 
ever  take  place  in  the  eggs  of  plants.  On  the  contrary  we  know 
that  the  first  cleavage-spindle  in  the  eggs  of  spermatophytes 
develops  without  centrosomes  from  a  mesh  of  fibrillae.  Also 
the  blepharoplasts  of  the  gymnosperms  Cycas,  Zamia,  and  Ginkgo 
remain  in  the  cytoplasm  at  a  distance  from  the  fusion  nucleus 
and  Shaw's  account  of  the  fern,  Onoclea,  indicates  that  similar 
conditions  obtain  there.  We  know  less  about  the  history  of  the 
blepharoplasts  within  the  egg  of  thallophytes  where  the  first 
cleavage-spindle  frequently  has  very  handsome  centrospheres 
and  asters  (e.  g.,  Fucus  and  Dictyota).  Strasburger  ('97a) 
pointed  out  that  one  of  the  asters  of  the  first  cleavage-spindle 
in  Fucus  arose  near  the  point  where  the  male  nucleus  united 
with  the  female.  However,  Farmer  and  Williams  ('98)  believe 
that  centrospheres  of  the  first  cleavage-spindle  in  Fucus  are 
formed  de  novo  and  Williams  (:  O4b)  came  to  the  same  conclu- 
sion for  Dictyota.  There  are  some  very  interesting  features  in 
the  comparative  study  that  Williams  (:  <34b)  has  made  on  the 
development  of  the  first  segmentation  spindle  in  the  fertilized 
and  parthenogenetic  eggs  of  Dictyota.  The  spindle  in  the  par- 
thenogenetic  egg  is  multipolar  and  develops  from  an  intranuclear 
kinoplasmic  mesh  and  there  are  no  centrospheres.  But  in  the 
fertilized  egg  a  centrosphere  always  appears  at  the  side  of  the 
nucleus  and  apparently  divides  into  two  which  separate  until 
they  lie  at  opposite  poles  of  the  mature  spindle.  Yet  Williams 
after  a  very  careful  study  concludes  that  this  centrosphere  arises 
de  novo  and  believes  that  the  stimulus  of  fertilization  enables 
the  fusion  nucleus  to  form  a  centrosphere  external  to  itself,  a 
thing  which  is  not  possible  for  the  nucleus  of  the  parthenogen- 
etic egg. 

It  seems  then  probable  that  the  only  structures  of  the  sperm 
that  preserve  their  morphological  entity  in  the  fertilized  eggs  of 
plants  are  the  chromosomes.  Whatever  may  be  the  relation  of 
the  blepharoplast  and  other  cytoplasmic  structures  as  stimuli  to 
the  development  of  the  egg  they  cannot  be  regarded  as  fixed 
factors  in  the  problem  of  heredity.  It  is  very  probable  that 
they  introduce  valuable  food  material,  perhaps  important  fer- 


No.  463.]  STUDIES    ON  PLANT   CELL.—  VI.  463 

ments,  substances  of  great  service,  although  possibly  not  abso- 
lutely necessary  to  the  successive  metabolic  processes  which 
characterize  growth  and  development.  But  the  _fact  remains 
that  we  have  in  the  chromosomes  the  only  new  morphological 
elements.  And  the  progress  of  research  seems  ever  to 
strengthen  the  general  view  that  in  the  chromosomes  are 
contained  the  directive  rudiments  of  development  and  that 
they  are  the  bearers  of  hereditary  principles.  Nuclear  studies 
on  apogamous  forms  will  certainly  prove  of  great  interest  in  this 
connection.  We  have  reason  to  expect  some  very  important 
results  from  thorough  cell  studies  on  apogamy  and  apospory. 

The  best  developed  theory  of  fertilization  in  plants  is  that  of 
Strasburger  and  a  statement  of  his  views  should  precede  any 
comments  of  other  authors.  Strasburger  has  written  much  on 
the  phenomena  of  fertilization  ;  important  considerations  may  be 
found  in  his  papers  of  '94a,  b,  '9/c,  :  ooa,  b,  :oi,  and  :  O4a. 
Strasburger  points  out  that  the  protoplasm  of  the  egg  is  pre- 
dominately trophoplasmic  in  character  because  of  the  propor- 
tionately very  large  amount  of  cytoplasm  with  granular  inclusions 
that  are  evidently  food  material  or  the  products  of  metabolism. 
On  the  other  hand  the  cytoplasm  of  the  sperm  contains  rela- 
tively little  trophoplasm  and  much  kinoplasm,  especially  when 
the  sperm  is  a  ciliated  cell  with  a  large  blepharoplast.  As 
Strasburger  conceives  kinoplasm  to  be  the  active  substance  of 
spindle  formation,  -he  concludes  that  the  sperm  might  bring  to 
the  well  nourished  egg,  rich  in  trophoplasm,  the  substance  neces- 
sary to  start  the  mechanism  of  mitosis.  In  its  broad  aspects 
this  view  is  very  similar  to  the  celebrated  theory  of  Boveri,  1887, 
that  the  spermatozoon  supplied  the  animal  egg  with  the  centro- 
some  which  is  conceived  as  necessary  to  start  mitotic  processes 
and  that  the  egg  is  powerless  to  divide  before  fertilization 
because  it  lacks  such  a  structure. 

Another  feature  of  Strasburger's  views  (advanced  in  his  paper 
of  :  oob)  appears  to  have  grown  out  of  the  discovery  of  the  so 
called  "double  fertilization  "  in  the  embryo-sac  and  other  nuclear 
fusions  whose  sexual  significance  is  not  clear,  together  with  the 
phenomena  of  parthenogenesis  as  produced  experimentally  in 
many  studies  of  recent  years.  Strasburger  considers  that  two 


464  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

processes  are  involved  in  the  sexual  act.  The  first,  termed 
"vegetative  fertilization,"  is  simply  the  stimulus  to  growth 
which  results  from  the  fusion  of  two  nuclei  or  other  masses  of 
protoplasm.  The  second,  called  "generative  fertilization,"  in- 
volves deeper  factors  than  those  of  mere  growth  stimulus. 
These  lie  in  the  union  of  germ  plasm  of  diverse  parentage  with 
the  mingling  of  hereditary  racial  characters  and  individual  varia- 
tions and  the  establishment  of  a  new  organism  which  may  have 
possibilities  of  development  quite  different  from  the  parent  form. 
The  effects  of  "  vegetative  fertilization "  may  be  imparted  to 
protoplasm  artificially  by  chemical  and  physical  stimuli  as  has 
been  clone  in  the  numerous  experiments  of  Klebs  and  Loeb 
on  the  conditions  which  induce  parthenogenetic  development. 
"Generative  fertilization"  has  a  phylogenetic  significance  and  a 
background  which  is  entirely  apart  from  the  mere  vegetative- 
processes  of  cell  growth  and  division. 

It  is  apparent  that  Strasburger's  theory  is  open  to  the  same 
line  of  criticism  that  has  been  brought  against  the  universal 
application  of  Boveri's  hypothesis  that  the  spermatozoon  brings 
to  the  egg  the  agent  of  cell  division  as  a  centrosome.  The 
investigations  of  several  zoologists  indicate  that  one  or  both  of 
the  centrosomes  in  the  first  cleavage-spindle  may  be  derived 
from  the  egg  or  may  be  formed  de  novo  (see  Wilson,  :  oo,  pp. 
196,  208).  The  kinoplasm  of  the  plant  sperm,  whether  in  the 
form  of  a  blepharoplast  or  as  an  ill  defined  accompaniment  of 
the  sperm  nucleus  has  not  been  shown  to  take  part  in  the  forma- 
tion of  the  first  cleavage  spindle.  There  is  no  evidence  that  the 
blepharoplast  retains  its  organic  entity  in  the  egg  to  pass  over 
into  a  centrosome  or  centrosphere.  Of  course  the  kinoplasm 
which  lies  immediately  without  the  nuclear  membrane  of  the 
sperm,  and  there  is  sometimes  a  conspicuous  amount  of  this 
densely  granular  protoplasm,  must  merge  with  similar  kinoplasm 
associated  with  the  egg  nucleus  at  the  time  of  fusion.  For 
example  Miss  Robertson  (:O4)  and  Coulter  and  Land  (105) 
note  in  Torreya  that  the  sperm  nucleus  brings  to  that  of  the  egg 
a  large  amount  of  accompanying  kinoplasm  which  forms  an 
investing  layer  around  the  fusion  nucleus.  It  is  reasonable  to 
suppose  that  the  mixing  of  these  masses  of  kinoplasm  with  the 


No.  463.]  STUDIES   ON,  PLANT  CELL.—  VI.  465 

fusion  of  the  gamete  nuclei  would  give  material  for  a  larger  and 
more  highly  differentiated  nuclear  figure  in  the  first  cleavage  of 
the  egg. 

Williams'  ( :  040)  observations  and  conclusions  on  Dictyota 
are  especially  interesting  in  this  connection  for  he  shows  that  the 
first  cleavage-spindles  in  the  parthenogenetic  eggs  are  intranu- 
clear and  multipolar,  showing  no  dominant  kinoplasmic  centers 
while  the  fertilized  eggs  form  each  a  well  differentiated  centre- 
sphere  with  radiations,  exterior  to  the  nuclear  membrane,  which 
clearly  guides  the  whole  process  of  spindle  formation.  Williams 
does  not  hold  that  this  centrosphere  comes  as  an  organized  struc- 
ture from  either  sperm  or  egg  but  is  developed  de  novo  by  the 
fusion  nucleus  as  the  result  of  the  general  stimulus  of  fertiliza- 
tion. The  evidence,  then,  furnished  by  studies  on  fertilization 
in  plants,  indicates  that  the  chromosomes  alone  maintain  mor- 
phological independence  throughout  the  process  of  fertilization 
and  that  the  kinoplasmic  (archoplasmic)  elements  play  no  part  in 
the  phenomena  as  fixed  morphological  structures  but  simply  con- 
tribute their  substance  to  the  general  union  of  cytoplasm  with 
cytoplasm,  and  that  any  specialized  kinoplasmic  structures  of  the 
first  cleavage  spindle  are  formed  de  novo.  While  it  is  true  that 
the  sperm  brings  to  the  egg  much  kinoplasm  it  may  well  be 
questioned  whether  such  kinoplasm  is  a  necessary  factor  in  the 
formation  of  the  first  cleavage-spindle.  It  seems  more  proba- 
ble that  the  development  of  achromatic  structures  in  the  first 
mitosis  following  fertilization  is  due  rather  to  the  general  stimu- 
lus of  cell  and  nuclear  fusion  than  to  particular  structures  sup- 
plied by  either  sperm  or  egg. 

The  second  phase  of  Strasburger's  theory  of  fertilization  con- 
cerns a  separation  of  the  two  processes  in  the  sexual  act :  ( i ) 
the  mere  growth  stimulus,  "vegetative  fertilization,"  that  may 
be  expected  with  the  union  of  any  two  masses  of  protoplasm, 
and  (2)  the  clearly  defined  sexual  phenomena,  "generative  fer- 
tilization," which  lies  in  the  union  of  germ  plasm  of  different 
parentage  and  diverse  potentialities  and  which  leads  to  the 
inheritance  of  these  characteristics.  It  seems  clear  that  the  two 
processes  are  really  present  and  can  be  clearly  distinguished. 
But  it  may  be  strongly  questioned  whether  the  factors  charac- 


466  THE  AMERICAN  NATURALIST.       [Vou  XXXIX. 

terizing  the  first  (vegetative  fertilization)  should  really  be  con- 
sidered a  part  of  the  sexual  act.  Strasburger  regards  the  proc- 
esses of  "generative  fertilization"  as  essential  to  the  sexual  act. 
The  growth  stimulus  "vegetative  fertilization"  is  always  to  be 
expected  as  an  accompaniment  of  fertilization.  It  may  be  given 
to 'cells  in  other  ways  than  by  the  sexual  act  and  is  found  in  cell 
and  nuclear  fusions  which  for  phylogenetic  reasons  are  plainly 
not  sexual. 

The  experimental  work  of  recent  years  on  the  conditions 
determining  artificial  parthenogenesis  have  done  much  to  define 
the  sorts  of  factors  which  stimulate  growth  and  division  of  sexual 
cells  when  the  process  of  fertilization  is  suppressed.  Klebs  for 
plants  and  Loeb  for  animals  have  been  foremost  in  these  studies 
and  they  have  shown  that  what  seem  to  be  very  minor  changes 
in  the  environment  of  the  sexual  cell  may  suffice  to  give  a  gamete 
the  power  of  immediate  development  without  fertilization.  Thus 
the  egg  of  the  sea  urchin  will  develop  parthenogenetically  to  an 
advanced  stage  when  placed  for  a  short  time  in  sea  water  contain- 
ing magnesium  chloride  and  then  brought  back  to  normal  sea 
water.  Nathansohn  ( :  oo)  found  that  a  small  proportion  (about 
7  Jfe )  of  the  eggs  of  Marsilia  vestita  would  germinate  partheno- 
genetically when  the  megaspores  were  cultivated  for  24  hours  at 
the  rather  high  temperature  of  35°  C.  arid  then  left  to  continue 
their  development  at  27°  C.  There  are  then  a  number  of  fac- 
tors such  as  varying  osmotic  pressure,  temperature,  and  in  some 
cases  chemical  reagents  which  may  induce  gametes  to  further 
development  without  the  usual  sexual  processes.  These  reac- 
tions seem  to  be  of  a  similar  character  to  the  processes  in  that 
phase  of  sexual  reproduction  termed  "vegetative  fertilization" 
by  Strasburger.  They  give  the  stimulus  to  growth  but  without 
that  essential  feature  of  sexuality,  the  mingling  of  germ  plasm  of 
different  parentage  which  distinguishes  the  processes  of  "  gener- 
ative fertilization." 

It  seems  to  the  author,  for  the  sake  of  clearness,  that  we  are 
trying  to  include  too  much  under  the  term  fertilization.  If  the 
features  of  "vegetative  fertilization,"  i.  e.,  the  growth  stimulus, 
can  be  introduced  experimentally  as  in  artificial  parthenogenesis 
then  they  cease  to  be  fundamental  qualities  of  the  sexual  act. 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  467 

They  are  accompaniments  of  sexual  processes  which  may  always 
be  expected  but  nevertheless  are  not  the  essential  characteris- 
tics. The  essence  of  the  sexual  act  (fertilization)  is  the  union  of 
germ  plasm  with  such  possibilities  of  new  developments  as  come 
from  the  inheritance  of  mixed  characters  from  two  lines  of  ances- 
try. And  the  more  diverse  and  complex  are  the  characters  of 
the  parents  the  more  conspicuous  are  the  essential  features  of 
the  sexual  act.  Among  lowly  organisms  and  in  simpler  types  of 
sexual  processes  the  growth  stimulus  becomes  exaggerated  in 
our  attention  because  the  features  of  heredity  are  not  so  promi- 
nent as  in  the  higher  forms.  But  in  the  higher  groups  the 
varied  characters  of  offspring  express  clearly  the  subtle  factors 
concerned  with  the  mingling  of  diverse  germ  plasm  in  the  proc- 
ess of  fertilization  and  the  growth  stimulus  recedes  into  the 
background. 

For  these  reasons  it  seems  to  me  that  the  term  fertilization 
should  only  be  used  for  the  mingling  of  germ  plasm  with  the 
possibilities  of  new  combinations  in  the  potentialities  of  the 
resulting  sexually  formed  cell  and  that  the  growth  stimulus  should 
be  treated  as  an  accompaniment  but  quite  apart  from  the  essen- 
tials of  the  sexual  act.  And  for  these  reasons  I  was  careful  to 
include  in  Section  IV  under  the  caption  "  Sexual  Cell  Unions 
and  Nuclear  Fusions "  only  illustrations  in  which  the  sexual 
nature  of  the  phenomena  was  clearly  shown  by  applying  a  mor- 
phological or  phylogenetic  test  to  the  elements  concerned  in  the 
process  of  cell  fusion.  The  phylogenetic  test  seems  to  me  the 
only  sure  way  of  determining  the  sexual  nature  of  the  members 
of  a  cell  fusion  and  there  are  very  few  cases  in  which  there  can 
be  any  hesitation  in  deciding  whether  or  not  such  elements  are 
morphologically  gametes. 

I  included  under  "Asexual  Cell  Unions  and  Nuclear  Fusions" 
in  Section  IV  a  number  of  cases  in  which  the  sexual  nature  of 
the  act  is  under  dispute  for  the  reason  that  none  of  these  satisfy 
the  phylogenetic  test.  It  is  perfectly  clear  that  the  growth  stim- 
ulus is  a  conspicuous  feature  of  these  cell  and  nuclear  fusions 
and  that  in  this  feature  they  resemble  sexual  processes  but  this 
does  not,  to  my  mind,  make  them  acts  of  fertilization  or  the 
equivalent  of  sexual  processes.  The  union  of  sporidia  in  the 


468  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

smuts  and  of  yeast  cells,  the  fusion  of  nuclei  in  the  teleutospore 
and  basiclium  and  in  the  apogamous  development  of  ferns,  the 
double  fusion  of  polar  nuclei  and  multiple  nuclear  fusions  in  the 
embryo-sac  (Corydalis)  illustrate  phenomena  which  I  cannot 
regard  as  sexual  even  though  they  have  in  them  elements  asso- 
ciated with  sexual  processes  and  in  certain  caseS  may  be  substi- 
tutes for  a  former  sexual  act.  In  none  of  these  instances  can 
we  be  positive  that  the  nuclei  concerned  are  morphologically  and 
phylogenetically  gamete  nuclei.  This  point  was  discussed  in 
some  detail  in  Section  IV.  It  seems-  to  me  that  Blackman's 
(:O4a,  p.  353)  conception  of  the  cell  fusions  preceding  the  geci- 
dium  in  Phragmidium  as  "reduced  forms  of  ordinary  fertilization" 
or  Farmer's  (103)  explanation  of  apogamy  in  the  fern  "as  a  kind 
of  irregular  fertilization  "  leads  to  a  confusion  of  a  substitute 
process  with  a  true  sexual  act.  The  substitute  processes  have 
their  true  place  as  phenomena  of  apogamy.  They  can,  however, 
only  have  a  sexual  significance  if  they  represent  the  origin  of  a 
new  set  of  gametes  in  the  organism,  a  proposition  which  is  not 
likely  to  be  maintained  by  anyone. 

3.    SPOROGENESIS. 

We  are  employing  the  term  sporogenesis,  as  must  have  been 
apparent  in  preceding  divisions  of  this  paper,  to  designate  a 
characteristic  and  highly  specialized  type  of  spore  formation  that 
is  universal  in  all  plants  above  the  thallophytes.  The  process 
always  terminates  the  sporophyte  phase  in  ontogeny  of  these 
higher  plants,  and  is  especially  distinguished  as  the  period  of 
chromosome  reduction  in  the  life  history.  The  cell  activities  of 
sporogenesis  are  therefore  of  particular  interest,  and,  since  spore 
mother-cells  are  generally  large  and  their  nuclear  and  cytoplasmic 
structure  especially  clearly  differentiated,  we  have  perhaps  ob- 
tained more  knowledge  of  mitotic  phenomena  from  the  study  of 
these  elements  than  of  any  other  tissues  of  the  plant  body. 

The  reduction  phenomena  of  sporogenesis  have  been  estab- 
lished in  some  forms  of  the  thallophytes,  certainly  in  the  tetra- 
spore  mother-cell  of  Dictyota  (Williams,  :  O4a).  There  are  also 
reasons  for  suspecting  that  the  oospore  of  CEdogonium  and  the 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  469 

zygospores  of  Conjugates  on  germinating  present  similar  events. 
The  teleutospore  and  basidium  are  probably  also  the  seat  of 
chromatin  reduction  (Blackman.  :  O4b)  in  the  formation  of 
spores  either  directly  or  through  the  promycelium.  The  ascus 
holds  a  position  at  the  end  of  a  sporophyte  phase  which  suggests 
a  similar  relation  in  this  group  of  fungi.  Chromosome  reduction 
may  also  be  expected  in  the  tetraspore  mother-cell  of  the  Rho- 
dophyceae,  as  in  Dictyota,  but  this  subject  has  never  been  inves- 
tigated. There  are  occasional  red  algae  in  which  the  tetraspores 
are  sometimes  borne  on  the  same  plant  with  the  sexual  organs, 
conditions  which  may  be  difficult  to  explain  on  the  theory  that 
the  tetrasporic  plant  is  a  sporophyte.  Thus  Spermotliainnion 
turneri  on  the  American  coast  frequently  bears  both  procarps 
and  tetraspores  on  the  same  plant,  and  I  have  also  seen  cysto- 
carpic  plants  of  Ceramium  rubrum  some  of  whose  branches  con- 
tained tetraspores.  Lotsy  (:  O4a)  also  reports  similar  conditions 
in  Chylocladia  kaliformis.  The  other  extremely  varied  methods 
of  spore  formation  (zoospores,  conidia,  etc.)  in  the  thallophytes 
do  not  concern  the  present  discussion.  They  seem  to  have  no 
fixed  place  in  the  life  history  and  there  is  nothing  to  indicate 
any  relation  to  reduction  phenomena,  although  we  actually  know 
nothing  about  the  chromosome  history  among  these  lowly  forms. 
The  importance  of  sporogenesis  as  a  critical  period  in  the  life 
history  of  higher  plants  became  at  once  apparent  with  the  dis- 
covery that  fertilization  doubled  the  number  of  chromosomes  in 
the  nuclei  of  the  sporophyte  phase  and  that  the  double  number 
was  reduced  during  sporogenesis.  As  stated  in  our  account  of 
gametogenesis,  these  facts  were  first  established  for  a  number  of 
spermatophytes  by  the  work  of  Strasburger  ('84,  '88,  and  '94), 
Guignard  ('84,  '85,  and  '91),  and  Overton  ('93  a  and  b).  Guig- 
nard  ('91)  presented  for  Lilinm  martagon  the  first  complete 
account  of  the  number  of  chromosomes  in  the  life  history  of  a 
plant,  and  his  results  were  also  established  independently  by 
Overton  ('93  a  and  b).  Then  followed  confirmatory  investiga- 
tions among  the  bryophytes  in  the  work  of  Farmer  ('94,  '95  a, 
b,  c)  and  in  the  pteridophytes  by  Strasburger  ('94,  p.  294)  for 
Osmunda.  Since  1895  the  investigations  among  the  spermato- 
phytes have  so  multiplied  that  we  know  the  number  of  chromo- 


470  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

somes  in  sporophyte  and  gametophyte  for  more  than  fifty  forms. 
This  list  may  be  found  in  Coulter  and  Chamberlain's  recent 
text-book,  The  Morphology  of  the  Angiosperms,  1903,  p.  81. 
Farmer's  accounts  of  the  number  of  chromosomes  in  the  Hepaticae 
have  been  confirmed  and  extended  by  myself  (Davis,  '99,  :oia) 
and  by  Moore  (:O3).  The  more  recent  literature,  especially  as 
it  concerns  the  events  of  spindle  formation  in  the  mitoses  char- 
acteristic of  sporogenesis  has  been  treated  in  our  account  of  the 
spore  mother-cell  (Amer.  Nat.,  vol.  38,  p.  725,  Oct.,  1904). 

There  are  two  chief  periods  in  the  processes  of  sporogenesis 
as  illustrated  in  all  groups  above  the  thallophytes  :  ( i )  a  growth 
period  and  (2)  a  period  of  cell  division.  In  the  growth  period 
the  spore  mother-cells  become  differentiated  from  the  general 
sporogenous  tissues  through  a  great  increase  in  the  amount  of 
protoplasmic  material.  At  some  time  in  this  growth  period  the 
nucleus  of  the  spore  mother-cell  exhibits  the  phenomenon  of 
synapsis,  a  very  characteristic  event,  recognized  by  the  very 
much  contracted  condition  of  the  chromatin  network  in  the 
interior  of  the  nucleus.  Synapsis  is  believed  to  hold  fundamental 
relations  to  reduction  phenomena  as  the  time  when  chromosomes 
unite  with  one  another  in  pairs.  The  period  of  cell  division  fol- 
lows synapsis  and  is  characterized  by  two  mitoses  in  the  spore 
mother-cell,  the  second  following  immediately  upon  the  first,  and 
a  segmentation  of  the  protoplasm,  sometimes  by  two  successive 
divisions,  and  sometimes  by  a  simultaneous  cleavage,  into  four 
spores.  The  two  mitoses  present  certain  peculiarities  in  the 
structure  and  behavior  of  their  chromosomes  which  are  unlike 
the  events  of  typical  mitoses.  The  first  is  known  as  the  hetero- 
typic  and  the  second  as  the  homotypic  mitosis.  These  peculiar- 
ities have  been  recognized  for  a  long  time  and  have  furnished 
the  subject  of  much  investigation  and  contradictory  explanations. 
They  were  briefly  described  in  Section  III  (Amer.  Nat.,  vol.  38, 
p.  740,  Oct.,  1904)  but  recent  studies  of  Farmer  and  Moore 
(:  03,  :  05)  have  opened  again  a  discussion  which  seemed  closed 
at  that  time.  The  details  of  synapsis  and  the  heterotypic  and 
homotypic  mitoses  will  be  taken  up  under  the  caption,  "  Reduc- 
tion of  the  Chromosomes." 

Contrary  to  a  statement  in  Section  III  of  these  studies  (Amer. 


No.  463-]  STUDIES   ON  PLANT  CELL.— VI.  471 

Nat.,  vol.  38,  p.  726,  Oct.,   1904)  there  is  probably  a  deep  sig- 
nificance in   the   fact  that  two  mitoses  are  almost  universally 
present  in  the  spore  mother-cell  so  that  four  spores  are  formed. 
It   is  probable  that  these  mitoses  are  always  heterotypic  and 
homotypic,  although  this  fact  has  only  been  clearly  established 
in   comparatively  few  favorable  forms,  and  that  they  are  indis- 
pensable to  the  mechanism  of  reduction  phenomena.    The  latest 
accounts  describe  the  first  mitosis  as  the  separation  of  the  two 
portions  of  a  bivalent  chromosome,  that  is  of  two   chromosomes 
joined  either  side  by  side  or  end  to  end,  giving  it  a  unique  posi- 
tion among  the  mitoses  of  the   life  history.     According  to  these 
theories    the    two   mitoses  of    sporogenesis    are    features   of  a 
remarkable   mechanism    by    which   the  paternal  and    maternal 
chromatin  after  its  union  in  synapsis  may  become  distributed  in 
proportions  that  can  be  expressed  by  mathematical  ratios.     The 
peculiarities   of  the  homotypic  mitosis   depend  on  a  premature 
fission  of  the  daughter  chromosomes  of  the  heterotypic  division 
as  will  be  explained  in  the  next  portion  of  this  section.     Thus 
the  four  spores  are  the  result  of  these  peculiar  mitoses  and  have 
morphological  significance.     We  are  even  justified  in  suspecting 
that  the  groups  of  four  spores  when  found  in  the  thallophytes, 
as  the  tetraspores  of  Dictyota  and  the  red  algae,  the  four  spores 
formed  on  the  basidium  and  promycelium  and  the  four  spores  of 
nuclei    present    in  the  germinating  oospore  and  zygospore  of 
QEdogonium  and  the  Conjugates  indicate  the  presence  of  reduc- 
tion phenomena  simply  because  the  number  four  is  so  constant. 
Williams  (:  O4a)  for  Dictyota  and  Blackman  (:  O4b)  for  types  of 
the  Uredinales  have  discovered  clear  cytological  evidence  of  this 
reduction  phenomenon  but  we  know  nothing  of  the  chromosome 
history  in  other  types. 

We  have  already  referred  to  the  fact  (Section  III,  Amer.  Nat., 
vol.  38,  p.  743,  Oct.,  1904),  that  in  the  spermatophytes  the 
two  mitoses  characteristic  of  sporogenesis  are  very  close  to  the 
mitoses  which  differentiate  the  gamete  nuclei.  In  the  male 
gametophyte  of  the  Angiosperms  there  are  generally  only  two 
mitoses  between  the  events  of  sporogenesis  and  gametogenesis 
and  in  gymnosperms  there  is  a  somewhat  larger  and  variable 
number.  The  female  gametophyte  of  the  angiosperms  usually 


472  THE   A  ME  RICA  N  NA  TURA  US  T.       [VOL.  XXX I X . 

presents  three  mitoses  after  those  of  sporogenesis  before  the 
egg  nucleus  is  formed.  But  in  a  number  of  types  in  the  lily 
family  (e.  g.,  Lilium,  Tulipa,  Fritillaria,  Erythronium,  etc.),  the 
mitoses  of  sporogenesis  are  actually  included  in  the  embryo-sac 
and  the  very  next  mitosis,  which  is  typical,  differentiates  the 
egg  (see  Section  III,  Amer.  Nat.,  vol.  38,  pp.  741-744,  Oct., 
1904).  This  is  the  furthest  point  attained  in  the  reduction  of 
the  gametophyte  which  in  such  forms  actually  includes  but  a 
single  nuclear  division  in  its  history.  But  however  close  the 
mitoses  of  sporogenesis  come  to  those  of  gametogenesis  it  is 
perfectly  clear  through  the  long  phylogenetic  history  in  the 
lower  spermatophytes,  pteridophytes,  and  bryophytes  that  the 
two  are  morphologically  distinct  processes  and  are  always  sepa- 
rate. It  is  unfortunate  that  the  terms  spermatogenesis  and 
oogenesis  should  be  applied  to  processes  of  sporogenesis  as  has 
been  done  by  several  authors,  for  such  usage  involves  a  confusion 
of  two  events  which  phylogeny  clearly  shows  to  be  different  in 
origin  and  to  have  back  of  them  the  diverging  history  of  sporo- 
phyte  and  gametophyte  from  the  times  of  thallophyte  ancestry, 
the  most  remarkable  evolutionary  history  in  the  plant  kingdom. 
It  is  conceivable  that  some  plants  may  finally  reach  a  stage  in 
their  evolutionary  history  when  all  the  gametophytic  mitoses  in 
the  pollen  grain  and  embryo-sac  will  be  suppressed  and  the 
nuclei  resulting  from  sporogenesis  become  gamete  nuclei.  But 
it  is  clear  that  in  such  an  event  the  gametophyte  phase  would  be 
obliterated  and  we  should  have  an  entirely  new  type  of  life 
history.  There  would  then  be  only  one  organism  (derived  from 
the  sporophyte)  whose  gametes  would  be  formed  immediately 
with  the  differentiation  of  the  pollen  grain  and  embryo-sac. 
Such  an  organism  would  present  reduction  phenomena  with  the 
differentiation  of  the  gametes  and  its  type  of  life  history  would 
be  identical  with  that  of  animals.  We  should  look  for  such  a 
reduced  life  history  in  groups  related  to  forms  in  which  the 
mitoses  of  sporogensis  are  included  in  the  embryo-sac  and  the 
gametophyte  phase  is  represented  by  a  single  nuclear  division 
(e.  g.,  Lilium,  Tulipa,  Fritillaria,  Erythronium,  etc.).  Search 
among  some  of  the  most  highly  specialized  Monocotyledon?e  may 
actually  reveal  examples  of  the  complete  suppression  of  the 
female  gametophyte. 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  473 

The  speculative  possibilities  of  a  suppression  of  a  sexual  gen- 
eration and  the  assumption  of  sexuality  by  an  asexual  phase 
were  clearly  in  the  mind  of  Strasburger  when  he  suggested 
('9/j.b,  p.  852)  the  possibility  that  the  two  mitoses  characteristic 
of  oogenesis  and  spermatogenesis  in  animals  might  signify  the 
remains  of  a  former  sexual  generation  now  entirely  suppressed 
in  the  Metazoa.  This  suggestion  was  based  on  the  striking 
similarity  of  the  events  of  sporogenesis  in  plants  to  those  of 
gametogenesis  in  animals  and  on  the  history  of  sporogenesis  as 
shown  in  plant  phylogeny.  This  history  is  remarkably  clear  and 
there  can  be  no  question  but  that  the  phenomena  of  sporogenesis 
have  developed  as  the  result  of  sexual  processes  and  are  always 
associated  with  an  asexual  generation  (sporophyte).  It  is  also 
clear  that  the  ancestral  primitive  sexual  generation  (gametophyte) 
h:is  steadily  degenerated  until  now  it  is  almost  lost  in  such 
embryo-sacs  as  include  the  two  mitoses  of  sporogenesis  within 
their  history.  If  the  sexual  generation  should  become  entirely 
lost  the  life  history  of  a  higher  plant  would  present  the  same 
features  with  respect  to  the  period  of  chromosome  reduction  as 
that  of  an  animal :  there  would  be  but  one  organism,  the  homo- 
logue  of  the  sporophyte  which  would  produce  gamete  nuclei  with 
reduction  phenomena  previous  to  gametogenesis  just  as  in-  ani- 
mals. Several  authors  have  expressed  views  similar  to  Stras- 
burger's  suggestion  ('94-b,  p.  852)  or  carried  the  speculation  even 
farther  than  he.  Beard  ('95a,  p.  444)  along  these  lines  of  argu- 
ment combined  with  conclusions  from  Bower's  ('87)  studies  on 
apospory,  announced  a  belief  that  "  Metazoan  development  was 
really  bound  up  with  an  antitJietic  alternation  of  generations." 
Lotsy  (:O5,  p.  117)  expresses  unequivocally  the  view  that  the 
animal  body  represents  an  asexual  phase  (2x  generation)  and  that 
the  sexual  phase  (x  generation)  is  confined  to  the  sexual  cells. 
Chamberlain  (:c>5)  simultaneously  with  Lotsy  and  in  much 
greater  detail  presents  a  comparison  of  the  phenomena  of  sporo- 
genesis in  plants  with  gametogenesis  in  animals  tracing  the 
resemblance  in  the  events  of  chromosome  reduction  step  by  step 
and  states  his  belief  that  "animals  exhibit  an  alternation  of  gen- 
eration comparable  with  the  alternation  so  well  known  in  plants." 

This  is  not  the  place  to  consider  this  theory  in  detail  from  a 


474  THE   AMERICAN  NATURALIST.       [You  XXXIX. 

zoological  standpoint  since  it  bears  only  indirectly  upon  the 
material  of  these  papers.  Zoologists  have,  however,  discussed 
critically  Strasburger's  suggestions  (see  Wilson,  :  oo,  p.  275, 
and  Hacker,  '98,  p.  101).  The  difficulties  of  accepting  this 
view  of  a  possible  antithetic  alternation  of  generations  in  animals 
seem  insurmountable.  In  the  first  place  there  is  not  the 
slightest  evidence  of  antithetic  alternation  of  generations  in  the 
Metazoa  or  for  that  matter  anywhere  in  the  animal  kingdom. 
The  examples  of  alternation  of  generations  which  the  zoologists 
present  among  the  Ccelenterates  are  all  illustrations  of  homolo- 
gous generations  derived  from  buds.  There  is  no  indication  of 
spore  formation  comparable  to  the  process  in  the  higher  plants, 
so  far  as  I  am  able  to  judge,  in  any  group  of  animals.  And  also 
there  seems  to  be  accumulating  evidence  of  reduction  phenomena 
previous  to  the  development  of  sexual  cells  in  the  Protozoa 
which  is  essentially  of  the  same  character  as  in  the  Metazoa 
(see  Wilson,  :  oo,  pp.  227,  277,  and  Calkins,  :oi,  p.  233).  It  is 
very  interesting  and  remarkable  that  reduction  phenomena 
should  show  the  same  order  of  events  in  animals  and  plants  and 
the  facts  should  be  clearly  recognized.  But  I  cannot  follow 
those  botanists  who  carry  over  to  the  animal  kingdom  the 
phylogenetic  conclusions  which  are  so  clear  in  plants.  The 
remarkable  agreement  of  the  events  of  sporogenesis  in  plants 
with  gametogenesis  in  animals  appears  to  me  likely  to  prove 
only  another  illustration  of  similar  biological  phenomena  which 
have  evolved  independently  of  one  another,  an  illustration  com- 
parable with  the  independent  origin  of  sex,  of  heterospory,  and 
probably  even  of  the  sporophyte  generation  itself  (involving  the 
processes  of  sporogenesis)  in  various  groups  of  the  plant  king- 
dom. 

We  have  considered  this  comparison  of  reduction  phenomena 
in  plants  with  animals  chiefly  to  emphasize  the  clear  cut  mor- 
phology of  the  process  as  understood  by  the  botanist.  It  does 
not  matter  how  close  the  events  of  sporogenesis  may  come  to 
those  of  gametogenesis  in  the  higher  angiosperms,  the  whole 
background  of  plant  phylogeny,  which  is  wonderfully  clear  as  a 
whole,  shows  that  reduction  phenomena  are  the  product  of  the 
asexual  generation.  It  represents,  as  Strasburger  has  so  well 


No.  463-]  STUDIES   ON  PLANT  CELL.— VI.  475 

expressed  it  ('94a,  p.  288),  a  return  on  the  part  of  the  plant 
organism  in  each  life  history  to  the  condition  of  an  ancestral  sex- 
ual generation  (garnet ophyte).  Reduction  phenomena  in  them- 
selves are  not  the  result  of  a  gradual  evolution,  whatever  may 
be  the  complicated  history  of  the  sporophyte  generation,  for 
they  consist  always  in  the  sudden  reappearance  of  the  primitive 
number  of  chromosomes,  characteristic  of  the  generation  in 
which  sex  arose  (gametophyte).  The  cause  of  reduction  phe- 
nomena is  phylogenetic.  The  interval  that  may  separate  this 
phenomenon  from  the  responsible  sexual  act  varies  immensely  in 
the  plant  kingdom  according  to  the  evolution  of  the  groups  con- 
cerned. But  the  suddenness  of  the  appearance  of  sporogenesis 
tells  in  every  case  the  same  story  of  an  immediate  and  total 
change  in  the  potentialities  of  the  protoplasm  in  the  spore 
mother-cell,  a  change  which  can  only  be  understood  as  a  phylo- 
genetic process  deeply  seated  in  the  race. 

When  the  events  of  sporogenesis  in  plants  are  considered  as 
processes  of  spermatogenesis  or  oogenesis  we  disregard  the  most 
remarkable  historic  outlines  that  plant  phylogeny  can  present, 
to  the  confusion  of  clear  thought.  Botanical  science  may  well 
be  proud  of  its  achievement  in  outlining  with  such  exactness  the 
relations  that  the  critical  periods  of  gametogenesis,  fertilization, 
and  sporogenesis  bear  to  reduction  phenomena  and  too  great 
stress  can  hardly  be  laid  upon  the  importance  of  the  results. 

4.    REDUCTION  OF  THE  CHROMOSOMES. 

There  are  perhaps  no  activities  of  the  cell  which  have  been 
the  subject  of  more  investigation  and  discussion  than  those  of 
chromosome  reduction  in  animals  and  plants.  The  reasons  are 
clear.  The  events  of  gametogenesis  in  animals  and  of  sporogen- 
esis in  plants  have  the  deepest  significance  for  an  understanding 
of  the  organization  of  protoplasm  because  these  are  periods  when 
great  changes  are  made  evident  in  the  structure  of  the  cells  con- 
cerned and  at  the  same  time  in  their  potentialities.  We  are 
forced  to  conclude  that  some  of  the  structural  changes  at  least 
are  the  cause  of  the  new  potentialities  and  the  attempt  to  estab- 
lish the  cause  and  effect  has  been  one  of  the  most  fruitful  and 


476  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

interesting  subjects  of  cell  research.  Reduction  phenomena  also 
have  a  deep  phylogenetic  significance  whose  history  in  plants  at 
least  can  be  traced  with  a  remarkable  degree  of  exactness. 

We  are  confident  that  sporogenesis  in  plants  signifies  the  sud- 
den return  of  the  organism  to  the  condition  of  an  ancestral 
sexual  generation  with  the  reappearance  of  a  primitive  number 
of  chromosomes.  The  short  time  consumed  in  the  process  and 
the  details  and  precision  of  the  cell  activities  show  that  we  are 
dealing  with  phenomena  whose  complicated  mechanism  can  only 
find  explanation  in  a  long  phylogenetic  history.  In  the  study  of 
reduction  phenomena  and  fertilization  we  have  reached  the  con- 
clusion that  the  chromosomes  are  intimately  concerned  with  the 
transfer  of  hereditary  qualities  and  are  probably  the  chief  or 
even  the  sole  bearers  of  these  characters.  And  thus  we  enter 
upon  some  of  the  most  far  reaching  problems  of  biology,  those 
of  heredity,  hybridization,  and  the  basis  for  the  remarkable 
ratios  of  inherited  characters  which  Mendel  first  clearly  set 
forth. 

It  seems  quite  certain  for  both  animals  and  plants  that  numer- 
ical reduction  of  the  chromosomes  takes  place  through  an  asso- 
ciation of  the  paternal  and  maternal  chromosomes  in  pairs  to 
form  the  reduced  number  of  bivalent  chromosomes  (dyads).  We 
have  presented  in  Section  IV  ("  Sexual  Cell  Unions  and  Nuclear 
Fusions  ")  the  evidence  which  indicates  that  paternal  and  maternal 
chromosomes  do  not  unite  at  the  immediate  time  of  nuclear 
fusion  in  fertilization.  On  the  contrary,  in  all  higher  animals 
and  plants  the  paternal  and  maternal  chromosomes  are  believed 
to  remain  separate  throughout  the  long  series  of  cell  divisions  in 
the  new  generation  up  to  the  time  of  sporogenesis  in  plants  and 
gametogenesis  in  animals,  both  events  being  characterized  by 
reduction  phenomena.  The  fusion  of  the  chromosomes  takes 
place  in  the  growth  period  which  differentiates  the  spore  mother- 
cell  in  plants  from  the  archesporium  or  the  primary  gametocyte 
in  animals  from  the  preceding  gametogenous  tissue.  The  growth 
period  is  one  of  general  protoplasmic  accumulation  and  increase 
in  the  chromatin  content  of  the  nucleus,  and  is  especially  char- 
acterized by  that  peculiar  activity  in  the  nucleus  termed  synap- 
sis.  Evidence  is  accumulating  that  synapsis  is  the  characteristic 


No.  463.]  STUDIES   ON  PLANT  CELL —  VI.  477 

feature  of  that   period    when    the    number   of  chromosomes   is 
reduced  by  half. 

Synapsis  is  followed  very  shortly  by  the  two  mitoses  charac- 
teristic of  sporogenesis.  These  nuclear  divisions  ~have  given 
rise  to  a  lengthy  literature  in  which  well  known  investigators 
have  shifted  their  positions  more  than  once.  The  discussions 
have  centered  on  the  methods  of  fission  and  distribution  of  the 
reduced  number  of  bivalent  chromosomes  which  appear  in  the 
first  mitosis  following  synapsis.  Assuming  that  the  chromatin 
is  organized  into  smaller  units,  represented  by  the  chromatin 
granules  (chromomeres,  Fol,  1891),  which  compose  the  chromo- 
somes, it  is  at  once  apparent  that  these  finer  elements  may 
become  variously  distributed  according  to  the  structure  of  the 
bivalent  chromosomes  and  the  character  of  the  mitoses  of  sporo- 
genesis. Each  fusion  bivalent  chromosome  is  composed  of  two 
chromosomes  joined  (i)  end  to  end  or  (2)  side  by  side  or  (3)  it 
is  possible  that  the  chromatin  is  intricately  mixed  in  the  struc- 
ture. With  respect  to  the  mitoses  a  transverse  division  of  the 
fusion  chromosomes  might  be  expected  to  give  a  very  different 
proportionate  arrangement  of  the  maternal  and  paternal  chroma- 
tin  from  longitudinal  divisions.  Should  the  chromatin  granules 
differ  qualitatively  from  one  another  then  different  parts  of  a 
chromosome  might  be  expected  to  have  different  characteristics ' 
which  would  be  distributed  by  the  mitoses  of  sporogenesis  in 
various  proportions  or  ratios. 

It  has  long  been  known  that  the  mitoses  of  sporogenesis  pre- 
sent peculiarities  in  the  mode  of  division  and  arrangement  .of 
the  chromosomes  at  the  nuclear  plate  which  make  them  unlike 
the  typical  mitoses  of  cell  division.  These  peculiarities  have 
led  to  the  designation  of  the  first  mitosis  as  heterotypic  and  the 
second  as  homotypic,  terms  which  are  now  applied  by  both  bot- 
anists and  zoologists  although  we  have  now  a  much  more 
extended  knowledge  of  each  type  than  when  Flemming  first 
proposed  the  classification  in  1887.  We  described  the  charac- 
ters of  the  heterotypic  and  homotypic  mitoses  in  Section  III, 
"The  Spore  Mother-cell"  (Atner.  Nat.,  vol.  38,  p.  740,  Oct., 
1904),  and  will  presently  treat  them  further  since  some  papers 
of  the  past  year  have  opened  again  a  discussion  which  seemed 


478  THE  AMERICAN  NATURALIST.        [VOL.  XXXIX. 

closed  a  few  months  ago.  The  chief  points  of  issue  in  dis- 
cussions of  reduction  phenomena  have  centered  around  the  sig- 
nificance of  the  heterotypic  and  homotypic  mitoses.  A  typical 
mitosis  is  believed  to  present  merely  a  quantitative  division  of 
each  chromosome  into  two  halves  equivalent  in  their  potentiali- 
ties. The  evidence  for  this  view  lies  in  the  longitudinal  fission 
by  which  each  chromatin  granule  on  the  spirem  is  supposed  to 
divide  and  contribute  half  of  its  substance  to  each  daughter 
chromosome.  Can  there  be  a  qualitative  division  of  a  chromo- 
some by  which  one  of  the  parts  differs  in  character  from  the 
other,  and  are  there  such  divisions  at  the  time  of  sporogenesis 
in  plants  and  gametogenesis  in  animals  when  reduction  phenom- 
ena take  place  ?  These  have  been  the  chief  topics  of  dispute  in 
studies  of  this  character  for  two  decades. 

The  problem  then  ultimately  concerns  the  structure  of  the 
chromosome  and  the  reason  for  the  constant  reappearance  of  the 
number  characteristic  of  the  species  at  the  beginning  of  each 
new  gametophyte  generation.  All  the  prominent  theories  of 
heredity  assume  that  the  chromosomes  are  made  up  of  simpler 
elements  which  stand  for  characteristics  of  the  race.  These 
may  form  various  combinations  of  higher  orders  and  collectively 
give  the  qualities  of  germ  plasm.  The  simplest  members  that 
can  be  observed  in  such  a  series  of  structures  are  the  chromatin 
granules  (chromomeres)  which  may  be  found  at  almost  all  times 
in  the  nucleus  and  are  especially  conspicuous  when  arranged  in 
a  row  on  the  linin  thread  of  the  spirem.  Weismann  has  devel- 
oped the  most  complex  conception  founded  on  the  above  princi- 
ples and  with  the  most  elaborate  terminology.  Starting  with 
the  chromatin  granule,  which  he  named  an  id,  Weismann 
assumed  that  this  element  is  composed  of  still  smaller  structures 
called  determinants  and  biophores,  the  last  being  the  ultimate 
living  units.  Groups  of  ids  make  up  idants  or  chromosomes. 
The  id  was  conceived  to  possess  all  the  essential  characters  of 
the  specific  germ  plasm  concerned  but  ids  vary  somewhat  among 
themselves,  determining  thus  the  individual  variations  of  the 
species.  Therefore  a  chromosome  or  idant  will  have  a  varying 
structure  according  to  the  character  and  distribution  of  the  ids 
which  compose  it. 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  479 

When  a  chromosome  divides  longitudinally  so  that  each  id 
splits  in  half,  the  daughter  chromosomes  are  exactly  equivalent 
and  the  division  of  the  chromatin  is  merely  quantitative.  But 
should  a  chromosome  divide  transversely  then  two  sets  of  entire 
ids  would  be  separated  from  one  another  and  the  two  daughter 
chromosomes  would  differ  in  proportion  as  their  component  ids 
varied,  i.  e.,  the  division  of  the  chromatin  would  be  qualitative. 
These  conceptions  of  the  possible  structure  and  mode  of  division 
of  chromosomes  outline  the  basis  of  Weismann's  theory  of 
heredity  and  will  serve  to  illustrate  the  general  attitude  of  those 
biologists  who  approach  the  subject  from  the  standpoint  of  pre- 
formation,  although  none  have  cared  to  formulate  such  elaborate 
assumptions  as  Weismann.  However,  there  is  a  general  agree- 
ment among  biologists  of  this  school  that  elements  are  present 
in  the  chromatin  which  do  carry  hereditary  characters  and  that 
the  chromatin  granule  and  chromosome  have  a  definite  architec- 
ture and  organic  value  because  of  these  elements. 

Weismann's  theory  of  heredity  rests  on  an  interpretation  of 
the  complexities  of  mitosis  presented  by  Roux  in  1883.  Roux 
assumed  that  chromatin  was  not  homogeneous  in  structure 
throughout  the  nucleus,  but  differed  qualitatively  in  various 
regions.  The  elaborate  history  of  mitosis  with  the  formation 
and  division  of  the  chromosomes  and  their  distribution  through 
the  mechanism  of  the  spindle  seemed  inexplicable  to  Roux 
except  on  the  theory  that  portions  of  the  chromatin  represented 
specific  characteristics  which  were  sorted  and  distributed  accu- 
rately according  to  some  system.  There  could  be  no  need  of 
such  a  complicated  mechanism  as  mitosis  if  the  distribution  of 
the  chromatin  was  to  be  merely  quantitative  for  simple  direct 
nuclear  division  could  perform  that  operation  as  effectively  as 
mitosis.  Mitosis  then  became  a  device  for  the  qualitative  dis- 
tribution of  chromatin  as  well  as  quantitative  and  the  characters 
of  the  daughter  cells  were  determined  chiefly  by  the  specific  ele- 
ments which  were  given  to  one  or  the  other. 

Weismann  siezed  upon  Roux's  suggestion  of  a  possible  quali- 
tative distribution  of  chromatin  in  mitosis  and  this  assumption 
became  a  very  important  feature  of  his  theory  of  heredity. 
Weismann  postulated  two  methods  of  mitosis.  By  the  first  the 


480  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

chromosomes  are  assumed  to  split  longitudinally  into  equivalent 
halves,  which  are  the  facts  in  all  vegetative  or  somatic  mitoses 
so  far  as  is  known,  and  the  chromatin  is  distributed  quantita- 
tively. By  the  second  method  chromosomes  were  conceived  to 
split  transversely  so  that  one  half  is  carried  to  each  daughter 
nucleus,  and  if  the  two  ends  of  a  chromosome  differed  in  the 
character  of  their  fundamental  elements  (ids  and  determinants) 
the  chromatin  would  be  distributed  qualitatively.  Weismann 
prophesied  in  1887  that  this  second  type  of  nuclear  division 
(qualitative  mitosis)  would  be  found  and  ever  since  investigators 
have  steadily  searched  for  a  transverse  division  of  the  chromo- 
somes. They  have  been  reported  in  connection  with  the  mitoses 
of  chromosome  reduction  both  for  animals  and  plants  and  the 
history  of  these  investigations  forms  an  important  part  of  the 
subject  of  reduction  phenomena.  But  the  present  interpretation 
of  these  transverse  divisions  involves  the  consideration  of  factors 
that  were  unknown  to  Weismann  and  are  very  different  from  the 
significance  assigned  by  him.  The  effect  of  Weismann's  specu- 
lations, as  a  stimulus  to  investigations  in  these  lines  can,  how- 
ever, hardly  be  overestimated. 

Botanical  literature  dealing  with  the  two  mitoses  of  sporogene- 
sis  presents  a  confusion  of  statements  respecting  the  presence 
or  absence  of  a  transverse  division  of  the  chromosomes.  Stras- 
burger  has  changed  his  opinion  three  times.  In  his  early  studies 
Strasburger  ('95)  believed  that  the  chromosomes  divided  longi- 
tudinally in  both  mitoses  of  sporogenesis.  Then,  led  by  studies 
of  Mottier  ('97)  he  concluded  ('97b)  that  the  fission  of  the  chro- 
mosomes in  the  second  mitosis  was  transverse.  Almost  imme- 
diately, however,  Strasburger  and  Mottier  reverted  to  the  former 
opinion  that  the  chromosomes  divided  longitudinally,  a  view 
which  Strasburger  maintained  in  his  lengthy  considerations  of 
reduction  phenomena  in  igooa.  Finally  in  a  recent  paper 
(:  O4b)  Strasburger  gives  a  very  different  interpretation  of  the 
events  of  the  first  mitosis  (heterotypic),  based  on  the  study  of 
Galtonia,  and  in  general  agreement  with  the  most  recent  conclu- 
sions of  Farmer  and  Moore  (103).  Farmer  ('95b),  Farmer  and 
Moore  ('95),  Miss  Sargant  ('96,  '97),  Guignard  ('99a),  Gregoire 
('99),  Lloyd  (:  02),  and  Mottier  have  also  held  that  the  divisions 


No.  463.]  STUDfES   ON  PLANT  CELL.—  VI. 

of  the  chromosomes  in  the  mitoses  of  sporogenesis  were  longi- 
tudinal with  somewhat  varying  views,  however,  as  to  the  exact 
time  when  the  two  divisions  take  place.  On  the  other  hand 
Ishikawa  ('97),  Calkins  ('97),  Belajeff  ('98),  and  Atkinson  ('99, 
for  Trillium)  have  claimed  that  the  second  mitosis  presented  a 
transverse  division.  Dixon  ('95,  '96,  :  oo)  and  Schaffner  ('97) 
held  a  position  apart  from  all  these  investigators,  believing,  that 
the  chromosomes  of  the  first  mitosis  of  Lilium  resulted  from 
loops  whose  free  ends  became  appressed  or  twisted  together 
finally  separating  at  the  angle  of  the  loop  and  thus  constituting 
a  transverse  division  in  this  first  mitosis.  These  latter  observa- 
tions accord  with  the  latest  conclusions  of  Farmer  and  Moore 
(:  03)  and  Strasburger  (:  O4b).  Most  of  this  literature  is  reviewed 
in  detail  in  Strasburger's  paper  of  igooa.  We  shall  omit  an 
historical  discussion  of  this  early  work  for  the  entire  subject  is 
approached  from  quite  a  different  standpoint  in  the  series  of 
papers  which  have  appeared  in  the  past  three  years  (1903-05) 
and  which  give  hope  of  much  clearer  information  on  the  mitoses 
of  the  spore  mother-cell. 

The  remainder  of  this  treatment  of  "  Reduction  of  the  Chro- 
mosomes "  will  take  up  the  recent  papers  and  try  to  show  the 
drift  of  the  present  investigations.  These  papers  had  not 
appeared  when  the  author  described  the  behavior  of  chromo- 
somes during  mitosis  in  Section  II  (Amer.  Nat.,  vol.  38,  p.  445, 
June,  1904)  and  presented  the  account  of  the  spore  mother-cell 
in  Section  III  (Amer.  Nat.,  vol.  38,  pp.  726,  740,  Oct.,  1904). 
At  that  time  it  seemed  probable  that  Strasburger's  conclusions 
of  1900  held  true  for  all  plants,  namely,  that  the  chromosomes 
split  longitudinally  in  both  mitoses  of  sporogenesis  as  well  as  in 
all  other  mitoses  of  the  life  history.  Whejther  these  views  may 
have  to  be  materially  changed  in  the  light  of  the  most  recent 
work  is  now  a  matter  of  dispute.  Yet  the  ground  has  shifted 
so  frequently  in  these  perplexing  problems  that  it  is  hard  to  feel 
sanguine  of  final  conclusions  even  in  the  hopeful  situation  of  the 
present.  I  shall  take  up  the  events  of  sporogenesis  in  order, 
beginning  with  the  growth  period  and  synapsis  and  ending  with 
the  two  mitoses  of  the  spore  mother-cell. 

The  growth  period  always  extends  over  a  considerable  length 


482  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

of  time  and  may  occupy  even  weeks  or  months.  During  this 
interval  the  spore  mother-ceils  increase  to  many  times  the  size 
of  the  archesporial  cells  from  which  they  were  derived.  There 
is  an  immense  accumulation  of  protoplasmic  material  and  a  cor- 
responding increase  in  the  size  of  the  nucleus  and  its  chromatin 
content.  The  growth  may  be  continued  in  the  spores  after  the 
mitoses  of  sporogenesis,  as  is  characteristically  illustrated  in  the 
great  increase  in  the  size  of  the  megaspores  in  the  pteridophytes 
and  certain  embryo-sacs.  The  most  striking  nuclear  activity  of 
the  growth  period  preceding  the  mitoses  is  synapsis.  This  term 
is  applied  to  a  very  characteristic  gathering  of  the  chromatin  and 
linin  material  in  a  compact  tangle  or  ball  at  one  side  of  the 
nucleus  and  usually  near  the  nucleolus.  Nuclei  are  sometimes 
in  a  state  of  synapsis  for  several  days  or  perhaps  weeks  as  is 
shown  by  the  frequency  of  the  stage  in  sporogenesis.  Thus 
during  the  entire  period  of  sporogenesis  in  Anthoceros  from  the 
inception  of  the  spore  mother-cell  to  the  final  differentiation  of 
the  spores  (which  must  take  many  days)  the  period  of  synapsis 
occupies  from  one  eighth  to  one  sixth  of  the  entire  time  (Davis, 
'99,  p.  104).  Synapsis  has  proved  to  be  a  very  difficult  subject 
for  study  and  few  investigators  have  made  detailed  observations 
upon  its  events.  Some  have  claimed  that  synapsis  is  an  artifact 
due  either  to  poor  fixation  or  to  a  particularly  sensitive  condi- 
tion of  the  cell  nucleus  by  which  the  chromatin  was  especially 
susceptible  to  shrinkage  but  it  seems  certain  now  that  the 
phenomenon  is  entirely  normal.  Miss  Sargant  ('97, -p.  195)  has 
observed  synapsis  in  the  living  pollen  mother-cell  of  Lilinm 
mart  agon.  Anthoceros  presents  a  particularly  favorable  subject 
for  the  study  of  the  effects  of  fixing  fluids  on  spore  mother-cells 
because  one  may  present  all  stages  in  the  same  sporophyte  to 
identical  conditions.  In  a  series  of  experiments  on  this  form 
(Davis,  '99,  p.  97)  with  a  number  of  standard  fixing  fluids  I  have 
always  found  synapsis  at  exactly  the  same  period  in  sporogenesis 
and  at  no  other  time  in  the  process.  True  synapsis,  character- 
istic of  reduction  phenomena  must  be  carefully  distinguished 
from  other  somewhat  contracted  conditions  of  the  chromatin 
which  are  cccasionally  found  in  cells.  Thus  Miyake  {Annals  of 
Bot.,  vol.  17,  p.  358,  1903)  noted  the  resemblance  to  synapsis 


No.  463-]  STUDIES   ON  PLANT  CELL— VI.  483 

of  an  accumulation  of  granular  material  in  the  nucleus  of  the 
central  cell  of  Picea  and  other  cases  might  be  cited  which  super- 
ficially resemble  synapsis  but  have  no  fundamental  relation  to 
this  peculiar  nuclear  activity. 

Evidence  is  steadily  accumulating  that  synapsis  is  a  very 
important  period  of  sporogenesis.  Some  authors  hold,  as  will 
be  described  presently,  that  it  is  the  time  when  paternal  and 
maternal  chromosomes,  which  have  remained  separate  through- 
out the  sporophyte  generation,  become  associated  in  pairs  to 
give  the  reduced  number  of  the  gametophyte.  This  conclusion 
makes  synapsis  the  actual  period  of  chromosome  reduction  and 
the  two  succeeding  mitoses  become  merely  distributing  divisions 
of  the  newly  formed  chromosomes.  Montgomery  (:  01)  first 
suggested  for  animals  that  synapsis  involved  a  union  of  maternal 
and  paternal  chromosomes  in  pairs.  Other  views,  however, 
regard  the  reduction  of  the  chromosomes  as  merely  the  tempo- 
rary union  of  paternal  and  maternal  elements,  end  to  end,  to 
form  a  bivalent  chromosome  characteristic  of  the  first  or  hetero- 
typic  mitosis.  According  to  this  view  the  bivalent  chromosomes 
divide  transversely  so  that  the  halves  are  distributed  as  whole 
chromosomes  in  the  first  mitosis. 

Two  very  important  papers  on  reduction  phenomena  have 
appeared  this  year  (1905)  both  of  which  were  preceded  by  pre- 
liminary publications,  that  of  Farmer  and  Moore  (:  03)  and 
Allen  (:O4).  These  two  accounts  best  represent  the  attitude  of 
the  opposing  schools  and  will  be  made  the  chief  texts  of  our 
treatment.  The  fundamental  points  of  difference  concern  the 
events  of  synapsis  and  the  heterotypic  mitosis  while  there  is 
complete  agreement  in  the  general  interpretation  of  the  homo- 
typic  mitosis.  All  authors  have  reached  essentially  the  same 
conclusions  as  regards  the  purpose  and  final  results  of  the 
reduction  divisions  but  the  details  of  the  processes  of  synapsis  and 
the  prophaseof  the  heterotypic  mitosis  are  described  in  radically 
different  ways  by  various  investigators.  However,  as  has  been 
stated,  the  views  fall  into  two  groups  or  schools,  one  led  by 
Farmer  and  Moore  with  whom  Strasburger's  recent  paper, 
<l  Ueber  Reduktionsteilung "  (1.04)  expresses  essential  agree- 
ment. The  other  school  includes  Allen,  Rosenberg,  and  the 


484  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

botanists  of  the  Carnoy  Institute,  Gregoire  and  Berghs.  To 
the  writer  the  conclusions  of  the  second  school  seem  better 
founded  and  we  shall  present  them  first.  Allen's  last  paper 
(:O5)  gives  the  most  complete  statement  of  their  interpreta- 
tions. 

Allen's  conclusions  (:  03,  :O5)  are  based  on  the  study  of  the 
pollen  mother-cell  of  Lilium  canadense  and  his  account  of 
synapsis  in  this  form  is  of  great  interest  for  the  simplicity  of 
his  explanation  of  the  events  of  this  phenomenon  and  their  sig- 
nificance. The  nucleus  of  the  young  pollen  mother-cell  follow- 
ing the  last  mitosis  in  the  archesporium  and  previous  to  synapsis 
contains  a  network  of  large  irregular  masses  connected  by  fibers 
of  varying  thickness.  The  irregular  masses,  which  probably 
contain  both  chromatin  and  linin,  are  derived  from  the  chromo- 
somes of  the  previous  mitosis  but  these  structures  cannot  be 
recognized  in  the  resting  nucleus.  Nucleoli  are  present  among 
the  irregular  masses  or  chromatin  knots  but  are  readily  dis- 
tinguished from  them.  As  the  nucleus  grows  larger  the  cnVoma- 
tin  knots  become  more  widely  separated,  but  synapsis  does  not 
occur  until  it  has  reached  its  full  size. 

During  synapsis  the  reticulum  becomes  transformed  into  a 
definite  spirem.  The  fibers  connecting  the  chromatin  knots 
increase  in  length  and  become  more  uniform  in  thickness  while 
the  knots  become  less  conspicuous  as  though  their  material  were 
drawn  out  along  the  fibers.  The  fibers  of  the  reticulum  are  now- 
seen  to  arrange  themselves  in  pairs  and  a  general  contraction 
of  the  network  takes  place  which  is  the  beginning  of  synapsis. 
Allen  believes  that  this  contraction  is  associated  with  the  approx- 
imation of  the  fibers.  The  contracting  network  occupies  at  first 
the  center  of  the  nucleus  but  later  moves  to  the  periphery  where 
the  nucleoli  .may  be  found  flattened  against  the  membrane. 
There  is  now  a  continuous  spirem  in  the  nucleus,  plainly  com- 
posed of  two  slender  threads  lying  side  by  side  and  probably 
with  no  free  ends.  These  two  threads  often  run  closely  parallel, 
sometimes  loosely  twisted  about  one  another,  sometimes  in  con- 
tact and  apparently  fused  and  sometimes  rather  widely  separated. 
It  is  clear  that  the  double  nature  of  the  thread  is  not  due  to  a 
fission  but  that  two  independent  threads  are  developed  indepen- 


No.  463.]  STUDIES   OF  PLANT  CELL.—  VI.  485 

dently  out  of  the  reticulum.  The  two  threads  gradually  fuse  so 
that  in  older  stages  of  synapsis  the  nucleus  appears  to  contain  a 
single  relatively  thick  spirem  which  is  shorter  and  -more  loosely 
coiled  than  in  the  earlier  stages.  The  minute  structure  of  the 
threads  of  the  spirem  can  be  determined  by  careful  staining. 
They  consist  of  a  series  of  chromatin  granules  (chromomeres) 
imbedded  in  the  ground  substance,  linin.  As  the  two  threads 
fuse  the  chromomeres  generally  come  together  in  pairs  and  unite 
to  form  a  single  row  of  large  chromomeres  which  project  from 
the  side  of  the  larger  single  (fusion)  spirem. 

The  single  (fusion)  spirem  on  emerging  from  synapsis  becomes 
uniformly  distributed  throughout  the  nucleus.  There  appear  to 
be  no  free  ends  in  the  much  convoluted  and  looped  thread. 
Some  df  the  loops  become  fastened  to  the  periphery  of  the 
nucleus  but  there  is  no  regularity  in  the  number  of  loops  and  no 
relation  to.  the  number  of  chromatic  segments  that  are  formed 
later.  While  thus  evenly  distributed  the  single  spirem  under- 
goes a  longitudinal  fission  which  is  preceded  by  the  division  of 
each  chromomere.  This  is  the  first  longitudinal  fission  of  the 
spirem  which  is  well  known  through  the  descriptions  of  Guignarcl, 
Gregoire,  Strasburger,  Mottier,  and  others.  The  fission  is  not 
simultaneous  throughout  the  length  of  the  spirem,  for  some  por- 
tions remain  undivided  for  some  time  when  contiguous  parts  are 
plainly  split.  The  result  is  a  condition  very  similar  to  that  pre- 
sented just  before  the  fusion  of  the  two  systems  of  threads 
during  synapsis  which  produced  the  single  (fusion)  spirem.  It 
seems  probable  that  the  threads  which  become  separated  are 
morphologically  the  same  as  those  which  fused  during  synapsis 
although  the  union  at  that  period  seems  complete.  The  split 
spirem  remains  uniformly  distributed  throughout  the  nucleus 
exhibiting,  however,  a  tendency  to  become  somewhat  massed  in 
the  center  of  the  nuclear  cavity  leaving  fewer  loops  attached  to 
the  nuclear  membrane. 

The  split  spirem  now  segments  throughout  its  length  into  the 
reduced  number  of  chromosomes  (12)  characteristic  of  the 
heterotypic  mitosis.  The  segmentation  is  not  simultaneous,  but 
the  first  free  ends  appear  near  or  at  the  periphery  of  the  nucleus 
where  the  split  spirem  breaks  apart  at  the  loops.  As  segmen- 


486  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

tation  proceeds  the  number  of  loops  becomes  fewer  and  the  free 
ends  more  numerous.  Allen  finds  the  breaking  apart  of  the 
arms  of  the  loops,  whose  heads  are  at  the  periphery  of  the 
nucleus,  as  described  by  Schaffner  ('97)  and  Farmer  and  Moore 
(:O5),  but  cannot  accept  the  interpretation  of  these  latter 
authors  (to  be  described  presently).  Allen's  studies  show  that 
the  loops  are  the  points  of  separation  of  adjacent  split  chromo- 
somes and  not  a  point  where  the  spirem  bends  on  itself  to  form 
a  pair  of  chromosomes.  The  ends  of  the  split  chromosomes 
when  properly  stained  are  seen  to  be  distinct  even  though  they 
may  be  in  contact  or  apparently  fused.  At  the  time  of  the  seg- 
mentation of  the  split  spirem  the  two  threads  are  generally 
twisted  about  one  another. 

The  split  chromosomes  now  shorten  and  thicken,  the  num- 
ber of  twists  is  reduced  and  the  pairs  of  elements  take  on 
the  many  forms  characteristic  of  the  heterotypic  mitosis  and 
described  as  I's,  J's,  X's,  Y's,  V's,  and  O's.  These  chromo- 
somes of  the  heterotypic  mitosis  are  of  course  pairs  of  chromo- 
somes, i.  e.,  bivalent  chromosomes  or  dyads.  They  are  believed 
to  represent  morphologically  the  full  number  of  sporophytic 
chromosomes  (24)  now  associated  in  pairs  forming  the  reduced 
number  (12)  of  bivalent  chromosomes.  The  two  threads  which 
fuse  are  believed  to  represent  two  spirems  of  maternal  and 
paternal  origin  and  the  chromosomes  in  the  pairs  are  derived 
from  different  parents. 

Shortly  after  the  segmentation  of  the  spirem  the  sporophytic 
chromosomes  of  each  bivalent  element  or  dyad  may  show  evi- 
dence of  a  second  longitudinal  fission,  first  recognized  by 
Gregoire  ('99),  Guignard  ('99),  and  Strasburger  (:  oo)  which  is 
completed  during  the  metaphase  of  the  heterotypic  mitosis. 
The  evidence  consists  in  the  appearance  of  a  double  row  of 
granules  in  each  sporophytic  chromosome,  the  result  of  the 
division  of  the  chromomeres.  However,  these  chromomeres 
soon  become  indistinguishable  from  the  linin  and  the  chromo- 
somes appear  homogeneous  from  now  on. 

While  the  spindle  of  the  heterotypic  mitosis  is  being  organ- 
ized the  position  of  the  sporophytic  chromosomes  shifts  with  the 
development  of  the  spindle  fibers  until  they  are  brought  to  the 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  487 

nuclear  plate  still  grouped  in  pairs  as  dyads  (bivalent  chromo- 
somes). The  details  of  spindle  formation  and  the  heterotypic 
mitosis  do  not  concern  the  present  discussion  of  reduction  phe- 
nomena. The  reduction  has  occurred  with  the  formation  of  the 
dyads  and  the  mitosis  simply  distributes  the  24  chromosomes 
(generally  called  daughter  chromosomes)  which  are  believed  to 
be  the  morphological  equivalents  of  the  sporophytic  chromosomes 
that  entered  the  spore  mother-cell  from  the  archesporium. 

Just  before  the  separation  of  the  sporophytic  chromosomes 
during  metaphase  of  the  heterotypic  mitosis  a  longitudinal  fission 
appears  suddenly  in  each  element  -extending  almost>~the  whole 
length.  This  is  the  second  longitudinal  fission  as  interpreted 
by  Gregoire  ('99),  Guignard  ('99),  Strasburger  (:  oo),  Mottier 
(:  03),  and  others,  with  whom  Allen  is  in  full  agreement.  It  is 
of  course  a  premature  division  of  the  chromosomes  preliminary 
to  the  homotypic  mitosis.  The  second  fission  is  probably  com- 
pleted at  this  time  but  the  elements  of  each  pair  (formerly 
called  granddaughter  chromosomes)  remain  clinging  together  at 
one  end  by  a  peculiar  overlapping  of  the  hooked  tips  forming 
thus  a  V-shaped  pair  whose  apex  is  drawn  to  the  poles  of  the 
heterotypic  spindle.  The  daughter  nuclei  following  the  hetero- 
typic mitosis  are  not  in  a  true  resting  condition  and  the  chromo- 
somes while  forming  a  spirem  show  abundant  evidence  of 
independent  structure.  They  emerge  from  the  spirem  at  the 
prophase  of  the  homotypic  mitosis  as  the  same  morphological 
entities  (i.  e.,  as  V-shaped  pairs)  and  are  thus  brought  to  the 
nuclear  plate  from  which  they  are  distributed  generally  as  fairly 
straight  rods  to  form  the  nuclei  of  the  pollen  grains. 

Rosenberg's  (:  O3a,  :  O4a,  :  O4b)  studies  on  the  hybrids  of 
Drosera  furnish  further  evidence  that  the  chromosomes  from 
different  parents  fuse  in  pairs  during  the  prophase  of  the 
heterotypic  mitosis.  The  gametophyte  number  of  chromosomes 
in  Drosera  rotundifolia  is  ten  and  in  D.  longifolia  twenty  and 
those  of  the  former  species  are  larger  than  those  of  the  latter. 
The  sporophyte  number  in  the  hybrid  is  thirty  as  would  be 
expected.  At  the  heterotypic  mitosis  of  sporogenesis,  however, 
twenty  chromosomes  appear  in  the  hybrid,  half  of  which  are 
plainly  double  structures  and  consist  each  of  a  larger  and  a 


488  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

smaller  element.  During  this  mitosis  the  ten  double  chromo- 
somes divide  but  the  single  chromosomes  remain  entire  and 
either  pass  to  one  pole  or  the  other  or  are  left  out  in  the  forma- 
tion of  the  daughter  nuclei.  The  explanation  of  these  conditions 
must  be  that  ten  chromosomes  of  D.  rotundifolia  fuse  with  ten 
from  D.  longifolia  leaving  ten  of  the  latter  without  mates. 
Rosenberg's  last  paper  (:O4b)  on  Drosera  describes  in  consider- 
able detail  the  union  of  chromosomes  in  pairs  in  both  species  of 
Drosera  during  sporogenesis.  The  sporophytic  chromosomes 
which  at  first  are  scattered  throughout  the  nucleus  in  the  early 
prophase  of  the  first  mitosis  come  together  in  pairs  and  unite  so 
closely  that  there  is  hardly  a  trace  of  their  dual  nature  in  the 
resultant  larger  bivalent  chromosomes,  which  are  of  course  the 
gametophyte  number.  Rosenberg  is  very  positive  that  the  pairs 
of  chromosomes  are  preliminary  to  a  fusion  and  not  the  result  of 
a  fission  of  already  reduced  segments  of  a  spirem  thread. 
Rosenberg  believes  that  the  two  halves  of  the  bivalent  chromo- 
somes are  separated  in  the  first  (heterotypic)  mitosis  and  that 
each  splits  lengthwise  prematurely  during  the  first  mitosis  in 
preparation  for  the  second.  The  fused  bivalent  chromosomes 
then  appear  to  divide  twice  longitudinally  but  the  first  division 
may  be  only  a  separation  of  the  two  sporophytic  chromosomes 
that  entered  into  the  fused  pair. 

We  shall  consider  now  the  conclusions  of  Berghs  and 
Gregoire  of  the  Carnoy  Institute,  Louvain,  whose  publications 
have  appeared  practically  simultaneously  with  some  of  those 
which  we  have  just  discussed.  Berghs  has  published  three 
papers  (:O4a,  :O4b,  :  05)  treating  of  the  early  history  of  sporo- 
genesis in  Allium,  Lilium,  and  Convallaria,  and  concludes  from 
a  study  of  synapsis  that  the  spirem  immediately  preceding  the 
heterotypic  mitosis  arises  from  the  close  association,  side  by 
side,  of  two  delicate  threads.  These  threads  are  organized  pre- 
vious to  and  during  synapsis  and  their  coming  together  brings 
about  that  contraction  of  the  chromatic  material  characteristic 
of  synapsis.  The  threads  contain  sporophytic  chromosomes  of 
the  last  mitosis  in  the  archesporium.  The  apparent  longitudinal 
fission  of  the  spirem  which  precedes  the  heterotypic  mitosis  in 
the  spore  mother-cell  is  interpreted  as  being  these  two  threads 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  489 

which  are  believed  to  have  never  actually  fused  during  synapsis. 
The  reduced  number  of  segments  derived  from  the  spirem  pre- 
ceding the  heterotypic  mitosis  are  then  bivalent  Chromosomes 
composed  of  pairs  of  sporophytic  chromosomes  lying  side  by 
side.  The  heterotypic  mitosis  distributes  the  sporophytic 
chromosomes  in  two  sets  resulting  in  a  numerical  reduction 
of  their  numbers  by  one  half.  It  will  at  once  be  noted  that 
while  Berghs  and  Allen  have  independently  arrived  at  similar 
conclusions  respecting  the  structure  of  the  chromosomes  of  the 
heterotypic  mitosis  there  are  some  important  differences  in  the 
mode  of  origin.  Allen  reports  an  actual  fusion  of  the  two 
threads  (paternal  and  maternal)  during  synapsis  and  a  later 
fission  of  the  spirem  previous  to  the  heterotypic  mitosis.  But 
the  accounts  of  both  authors  have  much  in  common  in  their 
interpretation  of  the  structure  of  the  spirem  and  chromosomes 
of  the  heterotypic  mitosis  which  is  fundamentally  different  from 
the  accounts  of  Farmer  and  Moore,  and  Strasburger  to  be 
described  later. 

Gregoire  (:  04)  in  a  general  discussion  of  reduction  phenom- 
ena confirms  the  observations  of  Berghs  and  takes  a  very  posi- 
tive position  against  the  interpretations  of  Farmer  and  Moore 
and  Strasburger.  The  chief  features  of  his  conclusions  are  in 
harmony  with  the  results  of  Allen.  The  sporophytic  (somatic) 
chromosomes  are  believed  to  become  associated  in  pairs  by  the 
application  of  two  delicate  threads  throughout  their  length  during 
synapsis.  These  threads  are  believed  to  retain  their  autonomy 
and  never  actually  to  fuse  although  they  may  come  in  close  con- 
tact. Consequently  the  reduced  number  of  chromosomes  are 
pairs  of  sporophytic  chromosomes  which  have  retained  complete 
independence.  Allen,  on  the  contrary,  reports  a  complete  union 
of  the  two  threads  involving  the  fusion  of  chromomeres  in  pairs 
and  a  later  longitudinal  division  throughout  its  length  of  the 
single  (fusion)  spirem.  Gregoire  does  not  regard  the  heterotypic 
mitosis  as  a  true  nuclear  division  but  as  a  special  process  designed 
to  effect  this  numerical  separation  of  the  sporophytic  chromo- 
somes and  intercalated  between  typical  mitoses,  while  Allen 
would  apparently  treat  it  as  a  true  mitosis  and  regard  the  chro- 
mosome reduction  as  effected  by  the  fusion  of  two  sporophytic 
spirems  during  synapsis. 


490  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

Rosenberg  (:O5)  has  recently  published  a  general  review  of 
reduction  phenomena  based  on  studies  upon  Listera,  Tanecetum, 
Drosera,  and  Arum,  taking  a  position  in  essential  agreement  with 
Allen  and  the  investigators  of  the  Carnoy  Institute  and  in 
opposition  to  the  theory  of  Farmer  and  Moore  and  Strasburger. 
Rosenberg  does  not  quote  Allen's  preliminary  paper  (:  04)  which 
anticipates  his  conclusions.  He  finds  that  the  spirem  which 
emerges  from  synapsis  is  preceded  by  a  condition  when  the 
structure  is  clearly  made  up  of  two  threads  (spirems)  which  lie 
parallel  to  one  another.  These  two  threads  are  frequently 
joined  together,  and  in  places  spirally  twisted  but  here  and  there 
they  may  be  seen  to  be  entirely  separated  from  one  another. 
They  finally  form  the  single  spirem  which  follows  synapsis  and 
which  divides  into  the  reduced  number  of  chromatic  segments. 
But  the  chromatic  segments  throughout  the  entire  processes  are 
shown  to  be  double  in  structure  (bivalent  chromosomes),  /'.  *?., 
composed  of  two  chromosomes  lying  very  close  together  side  by 
side  or  even  united.  What  appears  to  be  a  longitudinal  fission 
of  the  chromatic  segments  of  the  spirem  immediately  preceding 
the  first  mitosis  is  really  then  a  line  of  union  along  which  the 
two  independent  threads  have  come  together.  The  phenomenon 
of  synapsis  consists  of  this  close  association  of  two  threads 
which  are  themselves  simple  spirems  into  a  double  spirem  which 
segments  into  pairs  of  sporophytic  chromosomes  each  of  which 
may  be  regarded  as  a  bivalent  chromosome. 

Farmer  and  Moore  published  a  preliminary  communication  in 
1903  which  aroused  much  interest  in  their  theory  of  chromo- 
some reduction.  The  full  account  (:  05)  has  recently  appeared. 
Their  studies  are  upon  Lilium,  Osmunda,  Psilotum,  Aneura, 
and  the  cockroach,  Periplaneta.  Lilium  and  Osmunda  among 
the  plants  were  given  chief  attention  and  since  the  lily  was 
the  type  studied  by  Allen  it  will  serve  best  to  contrast  the 
conclusions  of  these  two  investigators.  The  accounts  of  Allen 
and  Farmer  are  so  fundamentally  different  as  regards  the  events 
of  synapsis  and  the  prophase  of  the  heterotypic  mitosis  that 
it  seems  scarcely  possible  that  both  can  be  right  in  their 
respective  material,  Lilium  candidum,  Farmer's  type,  and  L. 
canadense  of  Allen's  description.  Farmer  and  Moore  intro- 


No.  463-]  STUDIES   ON  PLANT  CELL.— VI.  491 

duce  the  terms  "maiosis"  and  the  "maiotic  phase"  to  cover  the 
whole  series  of  nuclear  changes  included  in  the  heterotypic  and 
homotypic  mitoses.  The  maiotic  phase  is  regarded  _as_  similar 
in  its  essential  details  in  both  animals  and  plants  but  the  fact  of 
its  appearance  at  different  points  in  the  life  histories  precludes 
any  probability  of  relationship  in  such  widely  divergent  lines. 
The  events  of  synapsis  and  the  consequent  peculiarities  of  the 
heterotypic  and  homotypic  mitoses  are  considered  as  intercalated 
between  the  series  of  typical  mitoses  in  the  life  history. 

Farmer  and  Moore's  conclusions  for  Lilium  c (indicium  may  be 
briefly  summarized  as  follows.  A  definite  spirem  with  the 
chromatin  distributed  as  granules  appears  in  the  young  spore 
mother-cell  before  its  separation  from  neighboring  elements.  A 
"  first  contraction  figure  "  now  appears  and  the  spirem  thread 
becomes  densely  coiled  in  the  vicinity  of  the  nucleolus,  this  con- 
dition persisting  for  some  time.  Then  the  coils  of  the  spirem 
loosen  and  become  distributed  about  the  periphery  of  the  nuclear 
cavity,  from  the  point  of  contraction  as  a  center.  A  longitudi- 
nal fission  of  the  spirem  thread  then  appears,  the  chromatin 
granules  dividing  so  that  they  come  to  lie  in  two  parallel  rows 
on  the  edge  of  the  split  ribbon.  The  fission  is  irregular  and 
open  loops  appear  at  places.  The  spirem  then  shortens  and  the 
split  gradually  closes  up  and  becomes  very  difficult  to  recognize. 
Many  of  the  convolutions  of  the  thread  are  attached  to  the 
nuclear  membrane  while  the  remainder  form  a  tangle  in  the 
interior  around  the  nucleolus  which  is  believed  to  give  up  much 
of  its  substance  to  the  chromatic  portion  of  the  spirem.  Farmer 
and  Moore  then  fail  to  find  the  double  thread  and  its  union  dur- 
ing synapsis  to  form  a  single  (fusion)  spirem  which  is  a  funda- 
mental feature  of  Allen's  account. 

There  follows  then  a  stage  which  has  been  the  subject  of 
much  discussion.  According  to  Farmer  and  Moore  the  spirem 
thread  becomes  pulled  out  into  V-  and  U-shaped  loops,  shown 
with  especial  clearness  where  the  bend  of  the  loop  is  attached  to 
the  periphery  of  the  nuclear  membrane.  The  arms  of  the  V's 
then  come  to  lie  parallel  and  so  close  together  as  to  give  the 
appearance  of  a  fission  in  a  structure  which  is  really  the  result 
of  an  approximation  of  the  two  free  ends  of  what  was  a  loop. 


492  THE    AMERICAN  NATURALIST.        [VOL.  XXXIX. 

The  spirem  thread  thus  breaks  up  into  segments  which,  how-- 
ever,  lie  in  pairs  represented  by  the  V's  in  the  reduced  (gameto- 
phyte)  number.  The  pairs  are  bivalent  chromosomes,  each 
composed  of  two  sporophytic  chromosomes  which  were  arranged 
serially  on  a  single  spirem  thread.  The  pairs  are  not  always 
organized  through  the  approximation  of  the  arms  of  V-shaped 
loops  but  this  is  a  very  characteristic  type  of  structure.  The 
V's  have  been  interpreted  by  other  authors  as  the  approximation 
of  portions  of  the  spirem  thread  (Dixon,  '95,  '96,  :  oo)  or  the 
separation  of  their  free  ends  at  the  bend  of  the  loop  as  a  trans- 
verse division  of  a  reduced  number  of  looped  chromosomes  in 
the  heterotypic  mitosis  (Schaffner,  '97).  The  two  parts  of  the 
bivalent  chromosomes  (which  are  pairs  of  somatic  chromosomes) 
now  become  shorter  and  thicker  and  all  trace  of  the  original 
fission  of  the  spirem  thread  is  lost. 

The  essential  features  of  Farmer  and  Moore's  interpretation 
of  the  prophase  of  the  heterotypic  mitosis  are,  then  :  (i)  a  sin- 
gle spirem  with  the  sporophytic  chromosomes  arranged  serially, 
which  splits  only  once  longitudinally,  the  fission  afterward 
becoming  obliterated  when  the  chromosomes  are  organized, 
and  (2)  the  organization  of  bivalent  chromosomes  in  the  reduced 
number  largely  by  the  approximation  of  the  free  ends  of  loops 
which  entails  a  separation  at  the  bend  of  the  loops  of  the  two 
sporophytic  chromosomes,  giving  the  appearance  of  a  transverse 
division. 

The  heterotypic  mitosis,  then,  according  to  Farmer  and 
Moore  involves  merely  the  distribution  of  the  sporophytic  chro- 
mosomes arranged  in  pairs  (bivalent  chromosomes)  as  univalent 
elements  to  each  daughter  nucleus.  This  is  of  course  the  gen- 
eral conclusion  of  all  recent  investigators,  the  different  views 
being  the  result  of  varying  accounts  of  the  method  of  organiza- 
tion of  the  bivalent  chromosomes.  During  this  distribution  in 
the  heterotypic  mitosis  the  split  of  the  original  spirem  appears 
in  each  univalent  element  (sporophytic  chromosome)  and  the 
halves  open  throughout  the  greater  part  of  their  length  giving 
the  peculiar  V-shaped  daughter  chromosomes  so  characteristic 
of  this  mitosis  in  the  lily.  The  arms  of  these  V's  become  the 
daughter  chromosomes  of  the  homotypic  mitosis  which  are  thus 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  493 

formed  prematurely  during  the  heterotypic  as  was  first  described 
by  Gregoire  ('99).  However,  Gregoire  and  most  botanists  have 
considered  the  split  between  the  V's  as  a  second  longitudinal 
fission  of  the  original  spirem  in  the  spore  mother-cell  while 
Farmer  and  Moore  regard  it  as  the  reappearance  of  an  original 
single  fission.  This  view  of  Gregoire,  which  has  had  the  sup- 
port of  Guignard  ('99),  Strasburger  (:  oo),  and  Mottier  (:  03),  is 
the  theory  of  a  double  longitudinal  splitting  of  the  chromosomes 
previous  to  the  heterotypic  mitosis  and  is  also  maintained  in 
Allen's  (:  05)  recent  paper. 

The  homotypic  mitosis  brings  about  the  final  separation  of  the 
arms  of  the  V-shaped  longitudinally  split  univalent  (sporophytic) 
chromosomes  of  the  heterotypic  division.  The  fact  that  the 
arms  of  these  V's  finally  break  apart  at  the  ends  does  not  con- 
stitute a  transverse  division  as  has  been  claimed  by  some  earlier 
writers  (Ishikawa,  '97  ;  Calkins,  '97  ;  Belajeff,  '98  ;  Atkinson, 
'99,  for  Trillium).  The  peculiarities  of  the  homotypic  mitosis 
are  then  due  to  the  premature  fission  of  the  univalent  chromo- 
somes during  the  heterotypic.  As  a  type  of  nuclear  division  the 
homotypic  mitosis  is  not  fundamentally  different  from  the  typi- 
cal divisions  of  other  periods  of  the  life  history.  All  recent 
authors  are  in  agreement  on  this  interpretation  of  the  events  of 
the  homotypic  mitosis. 

Gregory  (:  04)  gives  an  account  of  sporogenesis  for  several 
leptosporangiate  ferns  and  accepts  Farmer  and  Moore's  explana- 
tion of  reduction  phenomena.  He  finds  the  same  sort  of  U- 
shaped  segments  in  the  reduced  number  at  the  heterotypic 
division  and  considers  them  bivalent  chromosomes  which  divide 
transversely  so  that  the  original  sporophyte  chromosomes  are 
distributed  in  two  sets  during  this  mitosis.  The  various  posi- 
tions assumed  by  the  limbs  of  the  U-shaped  segments  give 
appearances  very  similar  to  the  tetrads  described  in  the  hetero- 
typic mitosis  of  animals  and  which  Calkins  ('97)  reported  for 
Pteris  and  Adiantum  and  regarded  as  resulting  from  the  trans- 
verse division  of  the  halves  of  a  longitudinally  split  chromosome. 
Gregory  of  course  cannot  accept  the  conclusions  of  Calkins. 

Williams  (1043)  applies  the  theory  of  Farmer  and  Moore 
respecting  the  bivalent  character  of  the  chromosomes  in  the 


494  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

heterotypic  mitosis  to  his  studies  on  the  first  division  in  the 
tetraspore  mother-cell  of  Dictyota.  But  it  can  hardly  be  said 
that  his  account  offers  any  material  support  to  the  theory. 
There  is  a  clear  synapsis  stage  preceding  the  mitosis  in  this  form 
from  which  a  spirem  emerges  as  a  beaded  thread.  This  spirem 
then  becomes  split  longitudinally  and  later  the  chromosomes  are 
organized  and  show  a  longitudinal  fission.  The  form  of  the 
chromosomes  at  metaphase  of  the  first  mitosis  is  heterotypic,  a 
ring  form  being  prevalent,  and  Williams  concludes  that  it  is 
developed  by  the  bending  and  closing  of  the  free  ends  of  a 
loop.  The  events  of  synapsis  are  not  clearly  enough  known  to 
make  possible  a  comparison  with  the  accounts  of  Allen  and 
Berghs. 

We  are  now  ready  to  take  up  the  latest  conclusions  of  Stras- 
burger  (:O4b)  which  are  closely  associated  with  views  expressed 
in  a  recent  paper  of  Lotsy  (:O4).  Lotsy  gives  a  clear  state- 
ment, illustrated  with  many  diagrams  of  the  various  ways  in 
which  sporophytic  chromosomes  may  be  conceived  to  unite  in 
pairs  previous  to  the  first  mitosis  in  the  spore  mother-cell  and 
the  manner  in  which  the  resultant  bivalent  chromosomes  may  be 
divided  and  distributed  by  the  two  mitoses  of  sporogenesis. 
Lotsy  makes  parallel  comparisons  between  sporogenesis  in  plants 
and  gametogenesis  in  animals  and  proposes  the  term  "Gonoto- 
konten "  ("  Nachkommenbildner ")  for  the  mother-cells  which 
inaugurate  reduction  phenomena.  The  paper  presents  no  new 
observations  but  discusses  the  problems  of  reduction  in  their 
broad  aspects.  An  excellent  summary  is  given  by  Koenicke 

004). 

Strasburger's  (:  O4b)  most  recent  paper,  "  Ueber  Reduktionstei- 
lung,"  is  based  chiefly  on  studies  of  Galtonia  and  Tradescantia 
and  presents  an  entire  change  of  view  from  his  conclusions  of 
1900.  Galtonia  seems  to  be  a  very  favorable  form  for  study  since 
the  gametophyte  number  of  chromosomes  is  only  six  and  the 
structures  are  exceptionally  clearly  differentiated  in  the  spore 
mother-cells,  which  Strasburger  calls  "  Gonotokonten "  after 
Lotsy.  A  single  spirem  is  reported  to  split  longitudinally  but 
the  two  daughter  threads  remain  close  together.  The  spirem 
then  shortens  and  thickens  and  becomes  distributed  in  heavy 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  495 

loops.  It  finally  divides  into  six  segments  which  are  interpreted 
to  be  six  pairs  of  chromosomes  joined  end  to  end.  These  six 
segments  are  then  bivalent  chromosomes.  The  two  chromosomes 
of  each  pair  (segment)  finally  come  to  lie  side  by  side  in  various 
positions  by  the  bending  of  the  original  looped  segments  and  the 
separation  of  their  two  ends  in  the  middle.  The  halves  of  the 
six  bivalent  chromosomes  (segments)  are  distributed  by  the  first 
mitosis  so  that  there  is  the  effect  of  a  transverse  division  of  six 
chromosomes  at  this  time,  but  really  the  process  is  one  of  the 
distribution  of  twelve  chromosomes  in  two  sets  of  six  each. 
The  longitudinal  fission  of  the  spirem  thread  becomes  more  con- 
spicuous towards  the  end  of  the  first  mitosis  so  that  the  twelve 
chromosomes  become  partially  split  and  pass  as  V's  to  the  poles 
of  the  first  spindle  during  telophase.  This  premature  division 
is  preparatory  for  the  second  mitosis  (homotypic)  when  the  sepa- 
ration is  finally  effected.  There  is  then  only  one  longitudinal 
fission  of  the  original  spirem  in  the  spore  mother-cell  and  this 
prepares  the  chromosomes  for  the  second  mitosis,  which  differs 
only  from  the  typical  mitoses  in  the  premature  splitting  of  its 
chromosomes.  The  first  mitosis  is  merely  the  separation  of  pairs 
of  chromosomes  joined  end  to  end.  Strasburger  interprets  the 
conditions  in  Tradescantia  and  Lilium  in  a  similar  way  believing 
that  the  complications  there  simply  arise  from  a  more  involved 
looping  of  the  spirem  thread.  Strasburger's  account  of  Gal- 
tonia  then  supports  in  all  essentials  the  theory  of  Farmer  and 
Moore. 

Strasburger  in  the  same  paper  (:O4b)  gives  an  account  of 
synapsis  which  cannot  be  brought  into  harmony  with  that  of 
Allen.  The  chromatin  granules  are  reported  to  gather  during 
synapsis  into  as  many  centers,  which  he  names  "  Gamozentren," 
as  will  finally  form  the  reduced  number  of  bivalent  chromosomes 
(six  in  Galtonia).  The  "  Gamozentren  "  then  become  arranged 
and  drawn  out  into  the  spirem  which  emerges  from  synapsis. 
The  chromatin  granules  are  named  "  Gamosomen "  and  the 
bodies  formed  in  the  "  Gamozentren  "  which  afterwards  become 
the  bivalent  chromosomes  of  the  first  mitosis  are  called  "  Zygo- 
somen."  There  are  then  no  organized  chromosomes  during 
synapsis  and  no  place  in  Strasburger's  account  for  the  fusion  of 


496  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

a  fully  organized  paternal  and  maternal  spirem  as  described  by 
Allen.  The  identity  of  the  sporophytic  chromosomes  becomes 
entirely  lost,  according  to  Strasburger's  explanation  of  synapsis, 
and  the  chromatin  granules  ("  Gamosomen  ")  may  be  variously 
distributed  in  the  new  set  of  bivalent  chromosomes  ("  Zygoso- 
men  ").  These  "  Zygosomen  "  are  a  new  creation  in  the  cell. 
All  of  the  other  theories,  on  the  other  hand,  preserve  the  mor- 
phological entity  of  the  sporophyte  chromosomes  which  are  of 
course  of  maternal  and  paternal  origin  but  allows  their  distri- 
bution in  various  ratios  to  one  another  during  the  first  mitosis  of 
sporogenesis.  The  chromosome,  however,  remains  a  fixed  mor- 
phological structure  from  one  generation  to  another.  These 
are  fundamental  differences  which  have  a  vital  bearing  on  the 
discussion  of  hybridization,  which  will  follow  shortly,  since  one 
of  the  most  important  features  of  the  problems  concerns  the 
preservation  of  the  relative  purity  of  the  germ  plasm. 

The  chief  characteristics  of  the  two  theories  of  reduction 
may  be  summarized  as  follows  :  — 

(i)  According  to  Allen,  Rosenberg,  Berghs,  and  Gre"goire, 
the  phenomenon  of  synapsis  presents  a  close  association  of  two 
parallel  chromatic  threads  (probably  of  maternal  and  paternal 
origin)  which  finally  unite  to  form  the  spirem  that  precedes  the 
heterotypic  mitosis.  This  single  (fusion)  spirem  is  then  double 
in  nature  and  the  longitudinal  fission  which  follows,  is  the  sepa- 
ration of  the  two  threads  that  entered  into  its  composition.  The 
reduced  number  of  chromatic  segments  of  the  heterotypic 
mitosis  are  bivalent  chromosomes  or  more  precisely  pairs  of 
sporophytic  chromosomes  derived  from  the  two  (maternal  and 
paternal)  threads  of  the  synapsis  stage.  The  heterotypic  mito- 
sis distributes  the  sporophytic  chromosomes  in  two  sets  thus 
effecting  a  numerical  reduction  by  one  half.  The  sporophytic 
chromosomes  divide  prematurely  during  the  heterotypic  mitosis 
in  preparation  for  the  homotypic  thus  presenting  a  second  longi- 
tudinal fission  of  the  segments  derived  from  the  single  (fusion) 
spirem.  A  special  feature  of  Allen's  studies  is  the  fusion  of 
chromomeres  in  pairs  during  the  organization  of  the  single 
(fusion)  spirem  and  a  subsequent  splitting  of  each  larger  chro- 
momere  with  the  longitudinal  fission  of  this  structure. 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  497 

(2)  Farmer  and  Moore,  Gregory,  Williams,  and  Strasburger 
hold  that  there  is  primarily  only  a  single  chromatic  thread  in  the 
nucleus  of  the  spore  mother-cell  which  is  the  spirem  of  synapsis 
and  the  heterotypic  mitosis  and  which  most  of  these  authors 
believe  to  be  composed  of  the  full  number  of  chromosomes 
(sporophytic)  joined  end  to  end.  This  spirem  splits  longitu- 
dinally but  the  fission  is  a  premature  division  which  prepares  the 
chromosomes  for  the  homotypic  mitosis.  The  chromosomes  of 
the  heterotypic  mitosis  are  formed  from  loops  of  the  spirem 
which  include  a  pair  of  sporophytic  chromosomes  joined  end  to 
end.  The  members  of  this  pair  come  to  lie  side  by  side  by  an 
approximation  of  the  arms  of  the  loops  and  a  breaking  apart  at 
the  head  of  the  structure.  This  transverse  fission  of  the  spirem 
is  not  of  course  a  transverse  division  of  a  chromosome  but 
merely  the  separation  of  a  pair  of  chromosomes  joined  end  to 
end.  The  line  between  the  two  arms  of  the  loop  marks  a  region 
of  contact  due  to  approximation  and  not  a  line  of  fission.  The 
heterotypic  mitosis  effects  a  numerical  reduction  of  the  chromo- 
somes as  in  the  first  view  but  these  chromosomes  are  formed 
on  entirely  different  principles.  A  single  premature  fission  of 
the  spirem  or  its  segments  prepares  the  chromosomes- for  the 
homotypic  mitosis. 

Comparing  the  two  schools,  it  may  be  noted  that  they  both 
explain  reduction  phenomena  as  a  numerical  reduction  of  the 
double  set  of  sporophytic  chromosomes  by  a  distribution  in  two 
sets.  The  fission  of  the  chromosomes  is  always  quantitative  and 
there  is  no  hint  in  any  of  the  views  of  a  qualitative  division  in 
Weismann's  sense.  Furthermore,  most  of  the  investigators  are 
firmly  convinced  of  the  individuality  of  the  chromosomes  which 
means  that  they  are  convinced  as  morphological  entities  persist- 
ing from  one  generation  to  the  next.  This  is  an  important 
agreement  in  relation  to  theories  of  heredity  and  hybridization 
which  we  shall  discuss  at  another  time  (see  treatment  of 
"Hybridization").  The  differences  lie  in  questions  of  fact 
regarding  the  organization  of  these  chromosomes  in  the  spore 
mother-cell  and  their  behavior  during  synapsis'  and  at  other 
periods  of  prophase  in  the  heterotypic  mitosis.  There  is  entire 
accord  in  that  the  chromosomes  of  the  homotypic  mitosis  appear 


498  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

during  the  metaphase  of  the  heterotypic  but  a  fundamental  dif- 
ference in  the  accounts  of  the  manner  in  which  these  structures 
are  formed. 

In  conclusion,  we  may  very  briefly  note  the  fact  that  the 
zoologists  are  divided  into  two  schools  in  their  accounts  of 
reduction  phenomena,  apparently  along  similar  lines  to  those 
of  the  botanists.  Some  recent  papers  (Winiwarter,  :  oo ; 
Schoenfeld,  :oi  ;  and  the  Schreiners,  -.04)  have  described  the 
union  of  parallel  threads  (maternal  and  paternal)  during  synapsis 
to  form  a  single  spirem  in  the  rabbit,  man,  bull,  hag-fish,  and 
shark.  Winiwarter  and  the  Schreiners  regard  a  later  longitudi- 
nal fission  of  the  spirem  as  a  separation  of  the  two  threads 
which  originally  entered  into  the  structure.  The  chromosomes 
in  the  hag-fish  (Myxine,  the  Schreiners,  :  04)  are  organized  in 
pairs  side  by  side  and  a  second  longitudinal  split  appears  in 
each.  The  heterotypic  mitosis  separates  the  groups  in  the  plane 
of  the  first  fission  and  the  two  parted  chromosomes  are  divided 
by  the  homotypic.  This  history  is  essentially  similar  to  Allen's 
account  of  the  lily.  On  the  other  hand  there  is  a  large  body  of 
observations  founded  on  the  investigations  of  Hacker,  vom 
Rath,  Riickert,  Montgomery,  and  others,  indicating  that  bivalent 
chromosomes  are  formed  consisting  of  somatic  chromosomes 
joined  end  to  end  and  that  these  elements  or  their  derivatives 
are  distributed  either  with  the  heterotypic  or  homotypic  mitosis. 
This  of  course  involves  a  transverse  division  which  is,  however, 
interpreted  as  the  separation  of  adjacent  chromosomes  and  not 
as  a  qualitative  division  in  Weismann's  sense.  The  attitude  of 
the  first  group  is  clearly  similar  to  that  of  Allen,  Rosenberg, 
Berghs,  and  Gregoire  among  the  botanists,  while  that  of  the 
second  shows  many  points  of  similarity  to  the  theory  of  Farmer 
and  Moore  and  to  Strasburger's  last  view  (:  04).  There  are  a 
number  of  accounts  of  a  double  longitudinal  fission  of  chromo- 
somes especially  among  the  vertebrates,  which  have  not  been 
harmonized  with  the  last  view  but  may  find  explanation  along 
the  lines  of  the  more  recent  investigations. 

It  is  of  course  conceivable  that  there  are  two  distinct  types  of 
arrangement  of  sporophytic  and  somatic  chromosomes  in  animals 
and  plants  at  synapsis  during  gametogenesis  and  sporogenesis. 


No.  463.]  STUDIES   ON  PLANT  CELL.—  VI.  499 

It  is  possible  that  they  may  be  grouped  in  pairs  (bivalent  chro- 
mosomes) either  side  by  side  through  two  parallel  threads 
(paternal  and  maternal  spirems)  or  end  to  end  in  a  siftgle  chro- 
matic thread.  But  it  will  certainly  be  interesting  if  animals  and 
plants  both  show  variations  in  these  respects  and  very  remark- 
able if  the  same  genus,  as  Lilium,  should  present  contrasting 
types  of  reduction  phenomena.  And  on  these  points  must .  be 
concentrated  the  future  investigations  in  this  field. 

While  we  are  making  progress  in  our  understanding  of  the 
behavior  of  the  chromosomes  it  must  never  be  forgotten  that  in 
them  we  are  dealing  only  with  the  most  conspicuous  form  of 
germ  plasm  and  that  there  are  much  finer  elements  which  in 
their  turn  will  demand  attention.  We  may  hold  to  the  view  of 
the  individuality  of  the  chromosomes  as  morphological  entities 
but  nevertheless  we  must  recognize  the  fact  that  the  substance 
of  these  bodies  which  stand  for  parental  characters,  the  idioplasm 
of  Nageli,  may  pass  through  remarkable  changes  which  are  far 
from  understood.  There  is  much  evidence  that  the  parental 
idioplasm  may  mix  or  combine  during  synapsis  in  the  organiza- 
tion of  the  spirem  from  which  are  developed  the  reduced  num- 
ber of  bivalent  chromosomes.  Allen  has  described  the  actual 
fusion  of  sets  of  chromomeres  believed  to  be  of  maternal  and 
paternal  origin  and  there  are  many  possibilities  of  the  two  idio- 
plasm s  reacting  upon  one  another  to  bring  about  intimate  and 
fundamental  interrelations.  These  become  important  principles 
in  discussions  of  heredity  and  hybridization  and  will  be  con- 
sidered later.  Allen  (:O5,  pp.  246-252)  presents  an  admirable 
analysis  of  these  problems. 


VOL.  XXXIX,  No.  464  AUGUST,  1905 

THE 

AMERICAN 
NATURALIST 


A   MONTHLY   JOURNAL 

DEVOTED  TO  THE  NATURAL  SCIENCES 
IN    THEIR    WIDEST   SENSE 


CONTENTS 

Page 

I.    A  Systematic  Study  of  the  Salicaceae  .       PROFESSOR  D.  P.  PENHALLOW  509 

II.    Developmental  Stages  in  the  Lagenidse       .       .       .       .       J.  A,  CUSHMAN  537 

III.  Studies  on  the  Plant  Cell.— VII DE.  B.  M.  DAVIS  555 

IV.  Notes  and  Literature:  Nature  Study ;  Zoology,  Wasps    Social   and   Soli- 

tary, Trouessart's  Catalogus  Mammalium,  Supplement 601 


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J.  A.  ALLEN,  PH.D.,  American  Museum  of  Natural  History,  New  York. 
E.  A.  ANDREWS,  PH.D.,/oAns  Hopkins  University,  Baltimore. 
WILLIAM  S.  BAYLEY,  PH.D.,  Colby  University,  Wattrville. 
DOUGLAS  H.  CAMPBELL,  PH.D.,  Stanford  University. 
J.  H.  COMSTOCK,  S.B.,  Cornell  University,  Ithaca. 
WILLIAM   M.  DAVIS,  M.E.,  Harvard  University,  Cambridge. 
ALES  HRDLICKA,  M.D.,   U.S.  National  Museum,  Washington. 
D.  S.  JORDAN,  LL.D.,  Stanford  University. 

CHARLES  A.  KOFOID,  PH.D.,   University  of  California,  Berkelty. 
J.  G.  NEEDHAM,  PH.D.,  Lake  Forest  University. 
ARNOLD  E.  ORTMANN,  PH.D.,  Carmgie  Museum,  Pittsburg. 
D.  P.  PENHALLOW,D.Sc.,F.R.M.S.,  Me  Gill  University,  Montreal. 
H.  M.  RICHARDS,  S.D.,  Columbia  University,  New  York. 
W.  E,  RITTER,  PH.D.,  University  of  California,  Berkeley, 
ISRAEL  C.  RUSSELL,  LL.D.,  University  of  Michigan,  Ann  Arbor. 
ERWIN   F.  SMITH,  S.D.,  U.S.  Department  of  Agriculture,  Washington 
LEONHARD    STEJNEGER,  LL.D.,  Smithsonian  Institution,  Washington. 
W.  TRELEASE,  S.D.,  Missouri  Botanical  Garden,  St.  Louis. 
HENRY   B.  WARD,  PH.D.,  University  of  Nebraska,  Lincoln. 
WILLIAM  M.  WHEELER,  PH.D.,  American  Museum  of  Natural  History, 
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STUDIES    ON   THE   PLANT    CELL.— VIL 

BRADLEY    MOORE    DAVIS. 

SECTION  V.     CELL  ACTIVITIES  AT  CRITICAL  PERIODS  OF 
ONTOGENY  IN  PLANTS  (Continued}. 

5.     APOGAMY. 

APOGAMY  is  the  suppression  of  the  sexual  act  and  the  devel- 
opment of  a  succeeding  generation  asexually.  The  term  was 
first  proposed  by  De  Bary  in  1878,  following  Farlow's  ('74) 
discovery  of  the  phenomenon  in  Pteris  cretica.  The  succeeding 
generation  may  arise  in  one  of  two  ways :  ( i )  by  the  develop- 
ment of  an  unfertilized  egg  or  gamete  which  is  termed  partheno- 
genesis, or  (2)  by  some  form  of  vegetative  outgrowth  from  the 
sexual  plant,  a  process  which  has  been  called  vegetative  apogamy. 
We  shall  not  attempt  to  give  a  detailed  account  of  apogamy  in 
the  plant  kingdom  but  will  confine  ourselves  chiefly  to  the  con- 
sideration of  a  few  detailed  studies  of  recent  months  which  have 
taken  up  the  cell  problems  concerned.  The  cell  problems  nat- 
urally treat  of  the  processes  which  may  be  substituted  for  the 
sexual  act  in  ontogeny  and  the  fundamental  problems  of  the 
behavior  of  the  chromosomes  under  these  conditions. 

Parthenogenesis  has  been  known  for  many  years  among  the 
thallophytes  which  furnish  illustrations  in  a  variety  of  groups. 
In  the  algae  we  have  the  well  known  examples  of  Chara  crinita, 
Cutlaria,  Dictyota,  some  species  of  Spirogyra  and  Zygnema,  and 
a  number  of  types  in  the  lower  Chlorophyceae  and  Phasophycese 
whose  motile  gametes  will  germinate  like  zoospores  should  they 
fail  to  conjugate  with  one  another.  The  recent  studies  of  Wil- 
liams (:04b)  on  Dictyota  give  the  only  observations  which  have 
been  made  on  nuclear  activities  during  the  parthenogenetic 
development  of  eggs  in  any  algal  form  and  will  be  considered 
presently.  The  fungi  furnish  beautiful  illustrations  of  partheno- 


556  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

genesis  in  the  Saprolegniales.  Trow  (:  04)  believes  that  some 
of  these  forms  are  sexual  but  there  can  be  little  doubt  that  the 
group  as  a  whole  is  generally  apogamous.  ^here  is  probably 
much  apogamy  in  the  Ascomycetes  and  an  almost  entire  suppres- 
sion of  sexual  organs  in  the  Basidiomycetes  but  no  clear  instance 
of  parthenogenesis  (i.  e.,  a  development  from  a  cell  whose  mor- 
phology is  unquestionably  that  of  an  egg)  is  known  in  either  of 
these  groups. 

Parthenogenesis  is  not  known  in  the  bryophytes  and  pterido- 
phytes  excepting  for  Marsilia  (Shaw,  '97;  Nathansohn,  :oo). 
Although  there  is  much  apogamy  in  the  pteridophytes,  especially 
in  the  leptosporangiate  Filicales,  the  new  generation  generally 
develops  as  a  bud-like  outgrowth  on  the  prothallus  (vegetative 
apogamy).  There  have  been  no  nuclear  studies  on  the  parthen- 
ogenetic  Marsilia  but  an  interesting  preliminary  account  has 
appeared  announcing  nuclear  fusions  in  the  apogamous  develop- 
ment of  Nephrodium  (Farmer,  Moore,  and  Digby,  :O3). 

Parthenogenesis  is  now  known  in  the  spermatophytes  for 
Antennaria  alpina  (Juel,  '98,  :  oo),  several  species  of  Alchemilla 
(Murbeck,  :oia,  :oib,  :  02  ;  Strasburger,  :  O4c),  TJialictrum  pnr- 
purascens  (Overton,  :  02,  :  04),  Gnetum  (Lotsy,  :  03),  a  number 
of  forms  of  Taraxacum  (Raunkiaer,  :  03  ;  Murbeck,  :O4),  sev- 
eral species  of  Hieracium  (Ostenfeld,  :  O4a,  :  O4b  ;  Murbeck,  :  04), 

Wikstrcemia  indica  (Winkler,  :O5),  and  is  suspected  for  Ficus 
Treub,  :O2)  and  Bryonia  dioica  (Bitter,  :O4).  A  number  of 
cases  of  polyembryony  were  formerly  considered  examples  of. 
apogamy  but  are  now  known  to  be  developments  from  the  nucel- 
lus  and  consequently  vegetative  buds  of  sporophytic  origin  and 
entirely  independent  of  gametophytic  activities.  The  best  known 
of  these  forms  are  Funkia,  Ccelebogyne,  Citrus,  Opuntia,  and 
Alchemilla  pastoralis.  Vegetative  apogamy  is  illustrated  in  the 
development  of  embryos  from  antipodal  cells  as  in  A I  Hum  odormn 

(Tretjakow,  '95  ;  Hegelmaier,  '97)  or  from  the  cells  of  the  endo- 
sperm as  in  Belanophora  (Treub,  '98  ;  Lotsy,  '99).  Synergids 
have  been  reported  to  form  embryos  in  a  number  of  forms  but 
many  of  these  have  proved  to  be  cases  in  which  the  synergic!  is 
fertilized  by  a  sperm  nucleus  and  not  examples  of  apogamy. 
However,  synergids  are  known  to  develop  embryos  apogamously 


No.  464.]  STUDIES  ON  PLANT  CELL.— VII.  557 

(or  parthenogenetically  if  the  antipodal  be  considered  the  homo- 
logue  of  an  egg)  in  Alchemilla  sericata  (Murbeck,  :  02).  A  sum- 
mary of  the  various  types  of  vegetative  apogamy,  parthenogen- 
esis, and  sporophytic  (nucellar)  budding,  supplementing  a  list  of 
Ernst  (:oi)  is  given  by  Coulter  and  Chamberlain  (:  03,  p.  221). 

We  will  now  take  up  the  few  investigations  which  consider 
the  cytological  details  of  parthenogenesis.  That  of  Williams 
(:  O4b)  on  Dictyota  is  the  only  one  treating  of  a  lower  type.  It 
seems  probable  that  parthenogenesis  in  Dictyota  is  in  no  sense 
normal  and  would  not  lead  to  mature  plants,  since  the  germina- 
tion of  unfertilized  eggs  in  the  cultures  of  Williams  presented 
many  irregularities.  The  spindles  instead  of  being  formed  from 
asters  with  centrosomes  are  intranuclear  in  origin,  multipolar, 
and  very  irregular  in  their  form.  As  a  result  the  16  chromo- 
somes become  scattered  and  a  cluster  of  daughter  nuclei  is 
formed  containing  varying  numbers  of  chromosomes,  sometimes 
one  and  sometimes  several.  It  is  clear  in  Dictyota  that  the  fer- 
tilization of  the  egg  results  in  the  development  of  an  aster  with 
a  centrosome  which  exerts  a  directive  influence  in  mitosis  pre- 
venting a  scattering  of  the  32  chromosomes  and  conducting  the 
mitosis  in  a  normal  fashion.  Williams  does  not  believe  that  the 
centrosome  is  introduced  as  an  organized  structure  into  the  egg 
by  the  sperm  but  that  it  is  formed  dc  novo  as  a  result  of  the 
increased  metabolic  activities  present  in  the  fusion  nucleus  as 
compared  with  that  of  the  unfertilized  egg. 

There  have  been  several  important  studies  on  parthenogenesis 
in  the  spermatophytes.  Some  of  these  papers  while  establishing 
the  facts  of  parthenogenesis  in  various  forms,  give  no  details  of 
nuclear  history  or  behavior  of  the  chromosomes.  But  the  studies 
of  Juel  (:oo),  Overtoil  (:O4),  and  Strasburger  (:  04),  present  some 
very  interesting  data  on  the  cytological  features  of  parthenogen- 
esis in  Antennaria  alpina,  Thalictrum  purpurascens,  and  several 
species  of  Alchemilla. 

Several  recent  papers  indicate  that  parthenogenesis  may  prove 
to  be  general  in  certain  genera  or  even  characteristic  of  large 
groups  and  therefore  a  far  more  widespread  phenomenon  than 
has  been  supposed.  Raunkiaer  (:  03)  (abstract  in  English  in 
Bot.  Centralb.,  vol.  93,  p.  81,  1903)  proved  by  cutting  off  the 


558  THE   AMERICAN  NATURALIST.       [VoL.  XXXIX. 

tops  of  young  flowers  that  several  species  of  Taraxacum  pro- 
duced normal  seeds  apogamously  and  concluded  that  the  embryo 
must  develop  parthenogenetically  since  Schwere,  in  1896,  traced 
its  origin  from  the  egg.  Ostenfeld  (:  043.,  :  040)  from  failure  to 
find  pollen  on  the  stigma  of  Hieracium  and  failure  to  make  it 
germinate  in  a  number  of  solutions,  was  led  to  try  similar  experi- 
ments to  those  of  Raunkiaer  in  cutting  off  the  anthers  and  stig- 
mas of  flowers.  He  found  that  a  large  number  of  species  of 
Hieracium  were  able  to  set  seed  apogamously  and  he  believed 
parthenogenetically  but  histological  investigations  were  not  made 
to  establish  the  last  point.  The  experiments  of  Raunkiaer  and 
Ostenfeld  are  interesting  as  showing  how  a  form  by  virtue  of  its 
parthenogenetic  habits  might  become  segregated  and  quite  re- 
moved from  the  probability  of  hybridization.  Murbeck  (:  04)  in 
a  short  paper  announced  that  the  embryos  in  Taraxacum  ancj 
Hieracium,  developing  from  flowers  whose  stamens  were  cut  out 
(as  in  the  experiments  of  Raunkiaer  and  Ostenfeld)  actually  do 
develop  from  the  egg  cell  and  are  therefore  parthenogenetic. 
Murbeck  also  failed  to  find  pollen  tubes  in  the  ovules  where 
pollen  had  been  applied  to  the  stigma.  Winkler  (:  04)  reports 
that  Wikstrcemia  indica  matures  very  little  perfect  pollen  and 
produces  its  seeds  apogamously,  as  proved  by  experiment.  The 
embryos  are  stated  to  develop  parthenogenetically  from  the  egg 
but  no  details  are  given  in  this  preliminary  paper  of  the  chromo- 
some history.  This  group  of  contributions  while  very  interest- 
ing, presents  no  data  on  the  fundamental  problems  in  a  cyto- 
logical  explanation  of  parthenogenesis. 

Murbeck  (:oia)  concluded  for  Alchemilla  that  true  tetrads 
were  formed  previous  to  the  differentiation  of  the  embryo-sac 
but  nevertheless  found  evidence  that  there  were  no  reduction 
phenomena  so  that  the  nuclei  within  the  embryo-sac  contain  the 
sporophytic  number  of  chromosomes.  Mur beck's  evidence  of 
tetrad  formation  was  not  satisfactory  and  in  the  light  of  recent 
studies  of  Strasburger  (:  O4c)  cannot  be  accepted.  His  view 
was,  however,  correct  that  there  is  no  reduction  of  the  chromo- 
somes in  the  formation  of  such  embryo-sacs  as  produced  par- 
thenogenetic embryos. 

Juel  (:  oo)  gives  a  critical  comparison  of  the  development  of 


No.  464.]  STUDIES   ON  PLANT  CELL.—  VII.  559 

the  embryo-sac  in  the  parthenogenetic  Antennaria  alpina  with 
A.  dioica  whose  ovules  are  normally  fertilized.  In  A.  dioica  the 
embryo-sac  is  one  of  a  group  of  four  cells  (tetrad )_which  are 
formed  through  two  successive  mitoses  (heterotypic  and  homo- 
typic)  showing  the  characteristic  features  of  sporogenesis.  A 
clear  stage  of  synapsis  precedes  the  first  mitosis.  The  type  of 
embryo-sac  development  in  this  form  is  then  entirely  normal. 
Not  only  are  tetrads  suppressed  in  the  parthenogenetic  Anten- 
naria alpina  but  there  is  no  trace  of  the  heterotypic  and  homo- 
typic  mitoses  in  the  embryo-sac.  The  number  of  chromosomes 
is  very  large  (about  fifty)  and  evidently  the  same  as  is  found  in 
other  periods  of  the  life  history.  There  is  then  no  reduction  of 
the  chromosomes  during  the  formation  of  the  embryo-sac  in  the 
parthenogenetic  species  and  the  egg  and  other  nuclei  in  this 
structure  have  consequently  the  sporophytic  number.  There  is 
no  need  of  fertilization  to  bring  the  egg  to  a  condition  when  with 
respect  to  chromosomes  it  is  prepared  to  develop  a  sporophyte 
embryo.  Juel  (:O4)  notes  certain  peculiarities  in  the  develop- 
ment of  the  embryo-sac  of  Taraxacum  officinale.  Tetrad  forma- 
tion is  reduced  to  a  single  mitosis  and  this  is  not  heterotypic, 
since  there  seems  to  be  no  reduction  of  the  chromosomes. 
Details  are  not  given. 

Overton  (:  04)  finds  normal  reduction  phenomena  in  the  pol- 
len mother-cell  of  Thalictrum  purpurascens  which  establishes  the 
number  of  chromosomes  to  be  24  for  the  sporophyte  and  12  for 
the  gametophyte  generations.  These  mitoses  are  thoroughly 
typical  of  sporogenesis  being  preceded  by  a  synapsis  stage. 
The  development  of  the  embryo-sac  is  of  two  types.  In  some 
cases  a  tetrad  of  four  megaspores  is  formed  from  a  megaspore 
mother-cell.  The  nucleus  of  this  cell  passes  through  a  synapsis 
and  the  first  mitosis  is  heterotypic  showing  the  reduced  number 
of  chromosomes.  The  lower  cell  of  the  tetrad  becomes  the 
embryo-sac.  But  many  embryo-sacs  pass  through  a  different 
history.  There  is  no  heterotypic  mitosis  and  no  reduction  of 
the  chromosomes  which  remain  24  in  number.  Thus  in  some 
ovules  the  mitoses  of  sporogenesis  are  omitted  and  true  tetrads 
are  not  formed,  with  the  result  that  the  embryo-sac  contains 
nuclei  with  the  sporophyte  number  of  chromosomes  (24)  in 


560  THE   AMERICAN  NATURALIST.        [VoL.  XXXIX. 

place  of  the  gametophyte  (12).  The  details  of  the  nuclear 
history  in  these  embryo-sacs  have  not  been  followed  but  it  is 
plain  that  their  eggs  have  the  requisite  number  of  chromosomes 
to  develop  sporophyte  embryos  parthenogenetically.  The  vary- 
ing proportions  of  parthenogenetically  developed  seeds  which 
may  be  found  on  plants  of  Thalictnim  purpnrascens  indicate  that 
the  suppression  of  normally  developed  embryo-sacs  is  not  very 
firmly  established  in  this  form. 

We  now  come  to  a  recent  paper  of  Strasburger  (:  O4c)  which 
is  the  most  important  contribution  to  the  subject  of  partheno- 
genesis that  has  yet  appeared.  Strasburger  studied  a  number 
of  species  of  Alchemilla  from  the  section  Eualchemilla,  the 
group  which  formed  the  subject  of  Murbeck's  important  discov- 
eries. Most  of  the  forms  develop  pollen  in  a  normal  manner 
and  Strasburger  was  able  to  follow  reduction  phenomena  in  this 
process  without  difficulty.  The  nucleus  of  the  pollen  mother- 
cell  passes  through  a  synapsis  followed  by  a  heterotypic  mitosis 
in  which  the  structure  of  the  chromosomes  as  bivalent  elements 
is  apparent.  The  bivalent  chromosomes  are  in  the  reduced 
(gametophytic)  number.  Similarly  Strasburger  found  that  some 
species  (c.  g.,  Alchemilla  pentaphylla,  gclida,  and  grossidens} 
formed  embryo-sacs  in  a  normal  manner  with  the  presence  of  a 
tetrad  and  a  characteristic  reduction  division  (heterotypic).  But 
the  development  of  the  embryo-sac  in  apogamous  species  (c.  g., 
AlcJicmilla  speciosa,  splendens,  and  fallax)  cuts  out  the  two 
mitoses  of  sporogenesis  and  no  tetrads  are  formed.  The  nucleus 
of  the  megaspore  mother-cell  emerges  from  synapsis  with  the 
sporophyte  number  of  chromosomes  and  the  first  division  which 
follows  is  a  typical  mitosis  and  not  heterotypic.  The  embryo-sac 
then  comes  to  contain  a  group  of  nuclei  with  the  sporophytic 
number  of  chromosomes  in  place  of  the  gametophytic  and  a 
parthenogenetic  development  of  the  egg  takes  place.  Stras- 
burger regards  the  parthenogenetic  tendencies  of  Eualchemilla 
as  associated  with  excessive  mutations  among  these  forms  through 
which  sexual  processes  are  becoming  displaced  by  apogamous 
methods  of  reproduction. 

This  clear  evidence  that  the  cause  of  parthenogenesis  in 
Antennaria,  Thalictrum,  and  Alchemilla  lies  in  the  suppression 


No.  464.]  STUDIES   ON  PLANT  CELL.— VII.  561 

of  chromosome  reduction  during  the  formation  of  the  embryo- 
sac  seems  to  offer  an  explanation  of  other  examples  of  apogamy 
presented  by  the  embryo-sac.  Thus  apogamous  devejojoments 
of  embryos  from  synergids  as  in  AlcJiemilla  sericata  (Murbeck, 
:  02)  or  from  antipodals  as  in  A  Ilium  odorum  will  not  seem 
strange  if  reduction  processes  are  suppressed  in  the  production 
of  an  embryo-sac  and  its  nuclei  retain  the  sporophyte  number  of 
chromosomes.  Such  nuclei  have  in  them  the  same  potentialities 
of  development  as  do  those  of  the  nucellus  whose  cells  form 
embryos  vegetatively  and  entirely  independent  of  gametophytic 
activities  in  a  number  of  forms  (e.  g.,  Funkia,  Ccelebogyne, 
Citrus,  Opuntia,  Alchemilla  pastoralis,  etc.).  This  type  of 
apogamy  from  a  gametophyte  which  retains  the  sporophyte 
number  of  chromosomes  may  be  found  to  hold  a  very  close 
relation  to  apospory  for  there  is  the  same  reduction  or  omission 
of  the  processes  of  sporogenesis  as  is  found  in  that  phenome- 
non. However,  since  we  know  nothing  of  the  cytological  events 
of  apospory  it  is  unwise  at  present  to  follow  the  speculation 
further. 

The  peculiarities  of  parthenogenesis  in  the  spermatophytes  do 
not  seem  so  remarkable  since  the  discoveries  recorded  above.  It 
is  not  strange  that  an  egg  should  form  an  embryo  without  fer- 
tilization when  its  nucleus  contains  the  sporophyte  number  of 
chromosomes.  The  most  remarkable  feature  in  this  suppression 
of  reduction  phenomena  in  Antennaria,  Thalictrum,  and  Alche- 
milla is  the  possibility  of  developing  an  embryo-sac  with  nuclei 
in  the  number  and  arrangement  typical  of  the  female  gameto- 
phyte and  yet  with  the  sporophyte  count  of  chromosomes.  The 
embryo-sacs  with  their  contents  have  clearly  the  morphology  of 
female  gametophytes  and  must  be  so  considered  in  spite  of  the 
fact  that  their  nuclei  contain  twice  as  many  chromosomes  as 
usual.  It  is  clear  that  the  potentialities  of  sporophyte  and 
gametophyte  involve  other  factors  besides  those  of  the  chromo- 
some count.  This  is  a  very  important  conclusion  because  we 
have  been  accustomed  to  lay  great  weight  on  the  number  of 
chromosomes  as  the  cause  of  sporophytic  and  gametophytic 
developments  respectively.  We  must  recognize  the  presence  of 
other  factors  determining  alternation  of  generations  besides  the 
chromosomes. 


562  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

There  are  two  types  of  parthenogenesis  in  plants  :  (i)  that  in 
the  thallophytes  where  there  is  no  sporophytic  generation,  and 
(2)  that  in  higher  forms  when  the  life  history  is  complicated  by 
an  alternation  of  generation.  We  know  nothing  of  the  cytologi- 
cal  conditions  in  the  first  group  including  such  types  as  Chara 
crinita,  Cutlaria,  some  species  of  Spirogyra  and  Zygnema  and 
numbers  of  the  lower  Chlorophyceae  and  Phaeophyceae  whose 
motile  gametes  will  germinate  like  zoospores  should  they  fail  to 
conjugate  with  one  another.  But  since  there  is  no  reason  to 
suppose  that  there  are  reduction  phenomena  at  gametogenesis, 
the  unfertilized  gamete  is  fully  prepared  with  respect  to  the 
number  of  chromosomes  to  continue  the  parent  stock.  Dictyota 
must  be  excluded  from  this  list  since  the  parthenogenetic  devel- 
opments here  are  abortive.  In  the  second  group  parthenogene- 
sis is  likely  to  prove  to  be  the  result  of  a  suppression  of  reduction 
processes  during  sporogenesis  by  which  a  gametophyte  genera- 
tion retains  the  sporophyte  number  of  chromosomes  and  in 
consequence  is  prepared  to  dispense  with  sexual  processes  in  the 
development  of  a  new  sporophyte.  Parthenogenetic  develop- 
ment in  animals  seems  to  be  similar  in  its  essential  cytological 
features  to  parthenogenesis  and  apogamy  in  plants.  There  may 
be  a  suppression  of  reduction  processes  somewhat  comparable  to 
that  discussed  above,  which  takes  place,  however,  at  the  time  of 
gametogenesis,  whereby  the  egg  nucleus  retains  the  number  of 
chromosomes  characteristic  of  the  parent.  Or,  through  a  fusion 
with  the  nucleus  of  the  second  polar  body  the  egg  nucleus  is 
brought  back  to  the  normal  condition  with  respect  to  the  num- 
ber of  chromosomes  of  the  parent  stock.  We  cannot,  however, 
consider  in  detail  the  forms  of  parthenogenesis  in  animals.  They 
have  been  recently  treated  by  Blackman  (:  O4b)  in  comparison 
with  conditions  in  plants. 

Apogamous  developments  which  involve  wholly  or  in  part 
other  elements  than  gamete  cells  and  nuclei  are  likely  to  be 
established  in  a  number  of  groups  of  the  thallophytes.  The 
author  has  long  believed  that  the  cystocarps  of  some  of  the 
Rhodophycese  develop  apogamously,  basing  his  conclusions  on 
certain  general  peculiarities  of  the  group  and  more  particularly 
on  a  study  of  Ptilota  (Davis,  '96).  Three  species  of  this  genus 


No.  464.]  STUDIES   ON  PLANT  CELL.—  VII.  563 

were  investigated  and  no  developments  from  the  carpogonia 
were  found,  but  the  cystocarp  in  all  cases  arose  from  a  cell  near 
the  base  of  the  group  of  procarps.  These  conditions  together 
with  the  rarity  of  male  plants  on  the  American  coasts  (none 
have  ever  been  reported)  give  strong  evidence  for  apogamy  in 
Ptilota.  There  are  a  number  of  genera  of  the  Rhodophyceae 
where  similar  conditions  seem  to  obtain  and  which  lead  one  to 
suspect  that  apogamy  may  not  be  very  exceptional.  However, 
the  subject  has  been  very  little  studied. 

As  is  well  known,  the  Ascomycetes  furnish  numbers  of  illus- 
trations where  ascogonia  have  not  been  found  or  appear  in  what 
seem  to  be  reduced  conditions  and  even  when  accompanied  by 
so  called  antheridial  filaments  these  latter  have  not  been  estab- 
lished as  functional.  De  Bary  recognized  the  possibility  of 
apogamy  in  the  development  of  the  ascocarps  of  these  forms 
and  very  little  critical  study  has  been  given  to  them  since  his 
time.  The  trend  of  investigations  in  this  group  has  been 
towards  the  more  interesting  problems  of  the  establishment  of 
sexuality  in  a  few  well  known  forms  (e.  g.,  Gymnoascus,  Sphae- 
rotheca,  Pyronema,  Monoascus,  and  among  the  lichens  and 
Laboul  beniaceae . ) 

It  is  generally  believed  that  no  sexual  organs  are  present  in 
the  higher  Basidiomycetes  (Autobasidiomycetes).  But  the 
recent  studies  of  Blackman'  (:  O4a)  in  the  Uredinales,  taken  in 
relation  to  the  well  known  nuclear  fusions  in  the  basidium,  pre- 
ceded by  a  mycelium  containing  paired  (conjugate)  nuclei,  make 
it  seem  very  probable  that  former  sexual  processes  in  the  Basi- 
diomycetes have  been  replaced  by  a  remarkable  type  of  apog- 
amous  development  of  a  sporophyte  generation.  Blackman  has 
traced  the  origin  of  the  paired  nuclei  in  the  Uredinales  (Phrag- 
miclium)  to  a  structure  preceding  the  aecidium,  a  structure. which 
seems  to  be  the  remains  of  a  female  sexual  organ.  We  will 
take  up  this  investigation  presently.  There  is  then  much 
reason  for  believing  that  a  sporophyte  generation  in  the  Basi- 
diomycetes arises  apogamously  in  the  creation  of  the  paired 
nuclei  and  terminates  with  their  fusion  within  the  teleutospore 
or  basidium. 

The  leptosporangiate  ferns  have  furnished  some  of  the  best 


564  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

illustrations  of  apogamy.  Since  Farlow's  discovery  in  1874  of 
an  asexual  sporophytic  growth  from  the  prothallus  of  Ptcris 
cretica  the  list  of  apogamous  pteridophytes  has  steadily  increased 
until  now  the  phenomenon  is  known  in  perhaps  25  forms.  Far- 
low's  investigation  was  followed  by  an  extended  study  of  De 
Bary  ('78)  on  a  large  number  of  forms  in  the  Polypodiaceas  and 
resulted  in  the  establishment  of  similar  sporophytic  outgrowths 
in  Aspidinm  falcatum  and  Aspidium  filix-mas  cristatitm.  De 
Bary  proposed  the  term  apogamy  ('78,  p.  479)  for  the  general 
phenomenon  and  distinguished  two  forms,  apandry  the  suppres- 
sion of  the  male  sexual  organs  which  results  in  a  parthenoge- 
netic  development  of  the  egg,  and  apogyny  for  the  suppression 
of  the  female.  Sadebeck  in  the  following  year  reported  apog- 
amy in  Todea  one  of  the  Osmundacese  (Schenk's  Handbnch  dei 
Botanik,  vol.  i,  p.  231,  1879)  thus  extending  the  phenomenon 
to  another  family.  And  later  apogamy  was  found  in  Tricho- 
manes  alatum  one  of  the  Hymenophyllaceae  (Bower,  '88)  and 
in  Selaginella  rupestris  (Lyon,  :O4,  p.  287). 

The  most  important  recent  contribution  on  apogamy  in  ferns 
is  by  Lang  ('98,  abstract  in  Annals  of  Bot.,  vol.  12,  p.  251). 
This  paper  presents  an  able  discussion  of  the  phenomenon  in 
its  relation  to  alternation  of  generations  and  adds  the  very 
interesting  discovery  of  sporangia  borne  directly  on  prothalli  that 
were  grown  from  spores.  These  sporangia  were  found  in  clus- 
ters on  a  thickened  lobe  or  process  from  the  prothalli  of  Scolo- 
pcndrinm  vnlgare  ramulosissimnm  and  Neplirodiwn  dilatmn 
cristatum  gracile.  The  sporangia  were  perfectly  normal  in 
structure  and  they  matured  spores.  It  is  probable  that  the 
process  is  itself  sporophytic  in  character,  i.  e.,  made  up  of  cells 
with  double  the  number  of  chromosomes  of  the  true  gametophy- 
tic  portion  of  the  prothallus,  but  cytological  details  are  not 
known.  Lang's  study  of  the  apogamous  development  of  sporo- 
phytic buds  on  several  forms  of  the  Polypodiacese  is  the  most 
detailed  work  on  apogamy  in  the  pteridophytes  yet  published. 
The  apogamous  growths  appeared  as  the  result  of  cultures  which 
were  watered  entirely  from  below  and  exposed  to  direct  sun- 
light, important  departures  from  normal  conditions  surrounding 
fern  prothalli.  In  all  cases  the  prothalli  developed  normal 


No.  464.]  STUDIES   ON  PLANT  CELL.—  VII.  565 

embryos  when  the  conditions  permitted  of  fertilization.  We 
shall  refer  to  some  general  considerations  of  Lang  in  our  sum- 
mary and  conclusions  on  apogamy. 

The  spermatophytes  present  some  exceedingly  interesting 
examples  of  apogamous  developments  of  embryos  from  nuclei 
within  the  embryo-sac  other  than  the  egg,  as  from  antipodals 
(Allium  odorwn,  Tretjakow,  '95  ;  Hegelmaier,  '97)  or  synergids 
(AlcJiemilla  sericata,  Murbeck,  :  02)  or  nuclei  in  the  endosperm 
(Belanophora,  Treub,  '98  ;  Lotsy,  '99)  but  in  these  cases  the 
sporophyte  number  of  chromosomes  is  apparently  present 
through  a  suppression  of  the  reduction  phenomenon  of  sporo- 
genesis  in  the  development  of  the  embryo-sac. 

We  will  now  consider  two  studies  which  describe  nuclear 
fusions  preliminary  to  the  appearance  of  apogamy  (Blackman, 
:O4a;  Farmer,  Moore,  and  Digby,  :O3). 

Blackman's  (:  O4a)  observations  on  Phragmidium  have  cleared 
up  to  a  great  degree  our  understanding  of  the  life  history  of  the 
Uredinales.  The  chains  of  secidiospores  have  been  found  to 
arise  serially  from  "fertile  cells"  which  form  a  group  at  the 
spot  where  an  aecidium  is  to  be  developed.  Each  fertile  cell 
has  above  it  a  sterile  cell  which,  however,  breaks  down.  The 
sterile  and  the  "  fertile  cell "  together  may  represent  a  female 
sexual  organ,  the  sterile  cell  perhaps  standing  for  the  remains  of 
a  receptive  structure  similar  to  a  trichogyne.  The  spermogonium 
consists  of  a  large  mass  of  antheridial  filaments  that  abjoint 
sperms  which  are  no  longer  functional.  It  is  of  course  uncer- 
tain whether  the  "  fertile  cells  "  are  morphologically  the  original 
female  gametes  since  they  may  readily  be  other  cells  drawn  into 
the  process  of  apogamy.  The  "  fertile  cell  "  is  stimulated  to 
activity  by  the  entrance  of  a  second  nucleus  either  from  an 
adjacent  hypha  or  from  the  cell  below.  The  second  nucleus 
does  not  fuse  with  the  original  nucleus  in  the  "fertile  cell  "  but 
the  two  come  to  lie  close  together  as  a  paired  or  conjugate 
nucleus.  The  two  nuclei  of  the  pair  divide  simultaneously 
(conjugate  mitosis)  throughout  a  long  series  of  nuclear  divi- 
sions, beginning  with  the  formation  of  aecidiospores  and  through 
the  vegetative  history  which  follows  up  to  the  production  of  the 
teleutospores  where  the  members  of  the  last  pairs  unite  to  form 


566  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

the  single  fusion  nuclei  within  these  reproductive  cells.  There 
is  much  evidence  that  the  period  in  the  life  history  characterized 
by  the  presence  of  paired  nuclei  represents  a  sporophyte  phase. 

Blackman  (:O4a,  p.  353)  regards  the  process  by  which  the 
second  nucleus  enters  the  "fertile  cell,"  resulting  in  the  conju- 
gate nuclei,  as  a  reduced  form  of  ordinary  fertilization.  I  have 
already  pointed  out  in  Section  IV,  "  Asexual  Cell  Unions  and 
Nuclear  Fusions,"  what  seem  to  me  to  be  serious  objections  to 
the  use  of  the  term  fertilization  when  it  is  clear  that  the  second 
nucleus  in  the  pair  is  morphologically  not  a  gamete  nucleus,  and 
the  subject  was  also  taken  up  in  the  account  of  fertilization  in 
the  present  section.  Whatever  may  be  the  physiological  inter- 
pretation of  this  remarkable  phenomenon  it  seems  to  me  clearly 
a  substitute  process  for  a  former  sexual  condition  and  involves 
other  elements  than  the  original  gametes  and  as  such  is  a  typi- 
cal illustration  of  apogamy. 

It  seems  probable  that  further  studies  in  the  Basidiomycetes 
will  determine  a  similar  origin  for  the  paired  nuclei  preceding 
the  basidium  to  that  of  Phragmidium  but  without  any  trace  of 
former  sexual  organs  at  least  in  the  higher  groups.  And  these 
conditions  must  signify  the  complete  disappearance  of  structures 
representing  sexual  organs  and  the  substitution  of  an  apogamous 
development  of  the  sporophyte  generation  for  the  sexual  act. 
In  this  connection  the  interesting  nuclear  fusions  in  the  ascus 
are  of  great  interest  for  they  may  hold  relations  to  degenerate 
sexual  conditions  in  the  Ascomycetes. 

Farmer,  Moore,  and  Digby  (103)  have  reported  some  remark- 
able nuclear  fusions  preceding  the  apogamous  development  of 
the  sporophytes  of  Nephrodium,  which  have  many  points  of 
resemblance  to  the  apogamous  phenomena  in  the  Uredinales 
just  described.  These  authors  find  that  cells  of  the  prothallus 
from  which  the  sporophytic  outgrowths  arise,  become  binucleate 
through  the  migration  of  nuclei  from  neighboring  cells.  The 
two  nuclei  may  remain  separate  for  some  time  or.  they  may  fuse 
at  once.  They  regard  the  whole  process  "  as  a  kind  of  irregu- 
lar fertilization  "  by  which  the  outgrowth  destined  to  form  the 
sporophyte  becomes  supplied  with  nuclei  containing  the  double 
number  of  chromosomes.  It  seems  to  me  unfortunate  to  asso- 


No.  464.]  STUDIES   ON  PLANT  CELL.—  VII.  567 

ciate  the  term  fertilization  with  this  phenomenon,  whatever  may 
be  the  physiological  significance  of  the  nuclear  fusions,  because 
we  are  not  dealing  with  gametes  and  there  cannot  be  involved 
in  the  process  anything  of  the  long  phylogenetic  history  of  sex- 
ual differentiation  in  the  group.  We  considered  these  matters 
in  some  detail  in  that  portion  of  this  section  entitled  u  Fertiliza- 
tion." 

With  respect  to  the  factors  which  determine  apogamy  it  must 
be  confessed  that  we  are  still  in  the  dark.  Lang's  ('98)  studies 
on  fern  prothalli,  however,  throw  some  light  on  the  problem.  In 
some  twenty  forms  of  the  Polypodiaceae  apogamy  resulted  when 
the  prothalli  were  kept  from  direct  contact  with  the  water  (i.  e., 
were  watered  from  below)  and  exposed  to  direct  sunlight. 
When  watered  from  above  these  same  forms  developed  normal 
embryos  from  eggs.  It  is  clear  that  the  suppression  of  condi- 
tions which  make  fertilization  possible  (i.  e.,  water  over  the  sur- 
face of  the  prothallus),  possibly  aided  by  sunlight  which  may 
cause  irregularities  of  growth,  induced  the  development  of  cylin- 
drical processes  from  which  the  apogamous  sporophytes  arose 
and  which  bore  sporangia  in  two  forms.  It  seems  hard  to  draw 
more  precise  conclusions  from  these  experiments  other  than  that 
the  normal  life  history  is  checked  at  a  critical  period  (fertiliza- 
tion) and  the  plant  is  forced  into  expressions  of  vegetative 
activity.  The  conclusions  of  Farmer,  Moore,  and  Digby  (:  03) 
offer  an  explanation  of  how  the  developments  may  take  on 
sporophytic  characters  through  the  fusion  of  nuclei  in  the  tis- 
sues and  the  establishment  of  a  sporophyte  number  of  chromo- 
somes. 

Strasburger  suggests  that  apogamy  in  Alchemilla  may  be  the 
result  of  a  weakening  of  sexual  power  associated  with  excessive 
mutative  tendencies.  This  would  seem  to  imply  that  excep- 
tional vegetative  activity,  with  the  appearance  of  much  variation 
under  favoring  conditions,  may  be  combined  with  apogamy.  It 
is  of  course  a  well  known  fact  that  a  high  degree  of  cultivation 
tends  to  lessen  the  fertility  of  a  form  unless  guarded  by  careful 
selection.  A  weakened  sexual  fertility  due  to  excessive  vegeta- 
tive activity  is  likely  to  be  replaced  by  forms  of  vegetative 
reproduction.  When  the  process  of  sporogenesis  becomes  so 


568  THE    AMERICAN  NATURALIST.        [VOL.  XXXIX. 

reduced  or  modified  that  the  female  gametophyte  retains  the 
sporophyte  number  of  chromosomes  as  in  the  embryo-sac  of 
Alchemilla  and  Thalictrum  the  apogamous  development  of  em- 
bryos is  to  be  expected. 

The  discovery  of  apospory  in  such  variable  and  perhaps 
mutating  genera  as  Alchemilla,  Taraxacum,  and  Hieracium  sug- 
gests quite  a  new  line  of  research  with  possibilities  of  a  clearer 
understanding  of  the  origin  of  mutations.  It  is  very  interesting 
that  these  widespread  and  successful  genera  should  give  evidence 
of  such  strong  apogamous  habits  for  it  seems  to  indicate  an  evo- 
lutionary tendency  in  the  higher  plants  of  great  significance. 
These  forms  with  Thalictrum  are  representatives  of  three  large, 
divergent  and  very  successful  orders  (Ranales,  Resales,  and 
Compositales)  and  it  suggests  the  probability  that  apogamy  will 
be  found  to  be  widespread  in  the  spermatophytes.  Its  bearing 
on  the  establishment  of  extreme  variations  and  mutations  may 
be  of  the  utmost  significance  for  it  is  clear  that  the  suppression 
of  sexuality  would  remove  sports  and  mutants  at  once  from  the 
swamping  effects  of  cross-fertilization.  The  sudden  appearance 
of  mutants  in  some  groups  and  their  ability  to  hold  true  may 
indeed  be  found  to  rest  on  the  establishment  of  apogamy  in  the 
form.  This  is  at  least  a  possibility  which  must  be  considered  in 
cytological  investigations  on  mutants  and  has  not  yet  received 
attention. 

The  subject  of  apogamy  touches  another  topic  of  importance, 
namely,  the  theory  of  homologous  generations  as  contrasted  with 
antithetic  generations  in  comparisons  of  sporophyte  with  gameto- 
phyte. We  shall  not  take  up  this  discussion  in  detail  here.  It 
must  have  been  apparent  to  the  reader  that  the  present  treat- 
ment of  the  critical  periods  in  the  life  history  of  plants  is  based 
on  the  conviction  of  the  correctness  of  the  latter  view  which  has 
had  the  support  of  Celakovsky,  Strasburger,  Bower,  Vaisey,  and 
Klebs.  The  theory  of  homologous  generations  as  held  by 
Pringsheim  and  Scott  is  admirably  discussed  by  Lang  ('98)  in 
connection  with  his  studies  on  apogamy  and  also  in  a  briefer 
note  (Annals  of  Bot.,  vol.  12,  p.  583).  Lang  seemed  inclined  to 
the  opinion  that  the  facts  of  apogamy  and  apospory  in  ferns 
lent  support  to  the  theory  of  homologous  generations  since  the 


No.  464.]  STUDIES   ON  PLANT  CELL.—  VII.  569 

prothallus  can  so  readily  take  on  sporophytic  potentialities  and 
the  sporophyte  develop  gametophytes  vegetatively.  But  Lang 
recognized  that  the  importance  of  this  evidence  woitkl— be  mini- 
mized should  it  be  found  to  depend  on  changes  of  nuclear  struc- 
ture. These  nuclear  changes  have  been  established  at  least  for 
apogamy,  either  in  the  suppression  of  the  reduction  phenomena 
of  sporogenesis  or  by  the  substitution  of  asexual  nuclear  fusions 
for  the  sexual  act,  and  the  argument  for  antithetic  alternation 
of  generations  seems  to  the  writer  stronger  to-day  than  ever 
before. 

6.    APOSPORY. 

Apospory  is  the  suppression  of  all  processes  of  sporogenesis 
and  the  development  of  a  gametophyte  generation  directly  from 
the  sporophyte.  The  term  was  first  proposed  by  Vines  (Jour, 
of  Bot.,  1878,  p.  355)  in  a  discussion  of  the  life  history  of  Chara 
and  adopted  by  Bower  ('86,  '87)  in  a  general  treatment  of  the 
subject  based  on  Druery's  ('86a,  '86b)  discoveries  of  prothalli 
developed  in  place  of  sporangia  directly  upon  the  leaves  of 
Athyrium  filix-fccmina  and  its  variety  clarissima.  The  phe- 
nomenon of  apospory  is  best  known  among  the  ferns  where  it 
has  been  most  extensively  studied  but  so  far  no  cytological  inves- 
tigations have  been  published.  Since  apospory  results  in  the 
development  of  a  gametophyte  generation  (presumably  with  the 
gametophyte  number  of  chromosomes)  without  the  preliminary 
process  of  sporogenesis  it  becomes  a  very  interesting  problem  to 
know  just  how  this  reduction  of  the  chromosomes  is  effected. 

Apospory  is  probably  not  uncommon  in  the  mosses  and  has 
also  been  reported  for  the  liverwort  Anthoceros.  The  inde- 
pendent studies  of  Pringsheim  ('76)  and  Stahl  ('76)  established 
the  facts  that  pieces  of  the  sporophyte  stalk  (seta)  of  Hypnum, 
Amblystegium,  Bryum,  and  Ceratodon  when  placed  on  damp 
soil  developed  a  protonema  which  in  its  turn  produced  leafy  moss 
gametophytes.  Stahl  also  found  in  Ceratodon  that  protonemata 
may  arise  from  the  capsule  wall  and  Brizi  ('92)  discovered  a 
similar  development  from  the  atrophied  capsule  of  Funaria 
hygrometrica.  Correns  ('99a,  p.  421)  has  confirmed  the  conclu- 


570  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

sions  of  Pringsheim  and  Stahl  in  species  of  Funaria,  Hypnum, 
and  Amblystegium  and  obtained  negative  results  in  a  number  of 
other  forms,  and  presents  an  excellent  review  of  the  subject. 
Lang(:oi)  discovered  that  small  pieces  of  the  sporophyte  of 
Anthoceros  la-vis  when  laid  on  damp  sand  produced  green  out- 
growths which  took  on  the  structure  of  young  gametophytes  and 
developed  rhizoids.  These  aposporous  gametophytes  most  com- 
monly arose  from  subepidermal  cells,  but  they  may  come  from 
any  layer  of  the  cortex  down  to  the  archesporial  cylinder.  It 
seems  probable  that  the  mosses  at  least  among  the  bryophytes 
are  able  to  reproduce  themselves  apogamously  without  difficulty, 
when  normal  processes  of  sporogenesis  are  interfered  with  and 
if  the  sporophytic  tissue  is  in  contact  with  moisture. 

The  leptosporangiate  ferns,  however,  furnish  the  most  con- 
spicuous illustrations  of  apospory  as  they  do  of  apogamy. 
Indeed,  the  two  phenomena  are  known  to  occur  in  the  same 
form  in  a  number  of  instances  (e.  g.,  AtJiyrium  filix-fcemina, 
NepJirodium  filix-mas,  Scolopendrium  vulgare,  Trichomanes  ala- 
tum,  etc.).  Beginning  with  the  discovery  by  Druery  ('86a, 
'86b)  of  apospory  in  Athyrium  filix-fcemina  and  its  variety 
clans sima  the  list  has  steadily  grown  until  now  apospory  is 
recorded  for  about  ten  forms.  In  Druery's  forms  the  prothalli 
developed  from  arrested  sporangia  and  the  spore  alone  is  left  out 
of  the  life  cycle.  But  Bower  ('86)  very  shortly  brought  forward 
in  Polystichum  angulare  pnlcherrimum  a  form  in  which  prothalli 
are  developed  as  simple  vegetative  outgrowths  from  the  tips  of 
the  leaves  and  the  life  history  is  thus  shortened  by  the  omission 
of  both  spores  and  sporangia.  This  condition  is  exactly  analo- 
gous to  the  development  of  protonemata  from  vegetative  cells  of 
the  sporophytes  of  mosses  and  Anthoceros.  The  following  year 
Bower  ('87)  presented  a  very  full  account  of  the  forms  of  Athy- 
rium and  Polystichum  just  described,  and  a  general  discussion  of 
the  phenomenon  of  apospory.  Bower  ('88)  then  extended  the 
illustrations  of  apospory  to  two  species  of  Trichomanes,  of  the 
Hymenophyllaceae  ;  Farlow  ('89)  reported  it  for  Pteris  aquilina, 
and  Druery  ('93)  in  Lastrea  pseudo-mas  cristata  and  ('95)  for 
Scolopendrium  vulgare  crispum.  The  exceptional  amount  of 
fern  variation  both  in  nature  and  under  cultivation  has  not  been 


No.  464.]  STUDIES   ON  PLANT  CELL.— VII.  571 

generally  appreciated  and  the  studies  on  apospory  and  apogamy 
indicate  that  much  of  it  is  associated  with  these  fundamental 
modifications  of  the  life  history  (Druery,  :oi). 

As  to  the  cause  of  apospory  we  are  as  much  in  the  dark  as  in 
the  case  of  apogamy.  The  phenomenon  is  clearly  associated  in 
some  forms  with  disturbances  in  the  normal  vegetative  life  of 
the  sporophytes.  This  is  particularly  true  in  the  cases  of  mosses 
and  Anthoceros  and  has  been  suggested  for  the  ferns.  Thus 
aposporous  developments  in  Pteris  aquilina  are  from  leaves  which 
are  generally  smaller  than  the  normal  and  whose  margins  are 
curled  so  that  the  leaf  often  appears  somewhat  withered  and  is 
easily  recognized  at  a  distance.  Bower  ('87,  p.  322)  is  inclined 
to  regard  the  phenomenon  in  the  ferns  as  a  sport  and  does  not 
consider  that  it  has  deep  morphological  significance  or  that  it 
offers  serious  difficulty  to  the  acceptance  of  the  theory  of  an 
antithetic  alternation  of  generations. 

As  we  have  stated  there  have  been  no  cytological  studies  upon 
apospory  but  there  seem  to  be  two  possible  explanations.  That 
which  is  likely  to  suggest  itself  first  calls  for  reduction  phenom- 
ena at  the  time  of  the  aposporous  development  by  which  the  nuclei 
of  the  sporophytic  tissues  may  come  to  contain  the  gametophyte 
number  of  chromosomes  and  are  therefore  capable  of  developing 
the  sexual  generation.  But  there  is  another  possibility  which 
has  not  yet  been  considered.  We  know  for  several  of  the  sper- 
matophytes  (Antennaria,  Juel,  :  oo  ;  Thalictrum,  Overton,  104; 
Alchemilla,  Strasburger,  :  O4c)  that  the  processes  of  sporogenesis 
may  be  suppressed  and  yet  a  structure  be  developed  with  the 
morphology  of  the  gametophyte  generation.  Thus  the  embryo- 
sac  will  contain  the  usual  number  of  nuclei  grouped  in  the  typ- 
ical manner  but  these  nuclei  still  have  the  sporophyte  count  of 
chromosomes.  It  seems  probable  then  that  the  development  of 
a  gametophyte  may  result  through  an  interference  with  the  nor- 
mal life  history  and  under  conditions  favorable  to  the  game- 
tophyte even  though  the  nuclei  retain  the  sporophyte  number 
of  chromosomes.  And  it  is  possible  that  some  of  the  aposporous 
developments  in  bryophytes  and  pteridophytes  may  be  of  this 
character.  It  is  quite  futile  at  present  to  carry  this  speculation 
further.  What  is  desired  is  some  cytological  facts. 


572  THE    AMERICAN  NATURALIST.       [VOL.  XXXIX. 

7.     HYBRIDIZATION. 

This  is  not  to  be  a  detailed  discussion  of  the  facts  and  theories 
of  hybridization,  a  subject  far  too  extensive  for  the  purposes  of 
our  treatment.  We  shall  only  consider  some  of  the  bearings  of 
the  recent  studies  on  fertilization  and  reduction  phenomena  upon 
the  problems  of  hybridization  treating  it  as  a  critical  phase  in 
the  life  history  of  the  organisms  concerned.  Until  recently  the 
attempts  to  formulate  definite  laws  for  the  formation  of  hybrids 
and  their  progeny  upon  a  physical  basis  have  not  been  satisfac- 
tory. But  the  work  of  a  number  of  breeders  all  of  whom  owe 
their  results  in  large  part  to  a  quick  appreciation  of  Mendel's 
epoch-making  contributions  have  brought  much  order  out  of 
what  was  a  very  confused  subject.  And  accompanying  the 
work  of  this  group  must  be  added  the  equally  important  con- 
clusions of  a  number  of  cytologists  whose  investigations  on  the 
structure  and  behavior  of  nuclei  in  the  critical  periods  of  fertil- 
ization and  chromosome  reduction  have  done  much  to  place 
Mendelian  principles  upon  a  cytological  basis.  We  shall  deal 
with  the  work  of  the  latter  group,  for  their  contributions  concern 
intimately  the  subject  matter  of  these  papers. 

We  shall  not  review  the  conclusions  of  Mendel  except  to  point 
out  the  relations  of  some  of  his  principles  to  cytological  phenom- 
ena. The  two  papers  of  Mendel  appeared  in  the  proceedings  of 
a  natural  history  society  of  Briinn,  Austria,  under  the  dates  1865 
and  1869.  They  lay  buried  until  1900  when  De  Vries,  Correns, 
and  Tschermak  independently  rediscovered  them  and  called  the 
attention  of  the  scientific  world  to  their  worth.  Soon  after, 
Bateson  published  a  translation  of  the  two  papers  (Menders 
Principles  of  Heredity,  Cambridge,  1902)  with  an  introduction 
and  a  defense  against  the  criticisms  of  Professor  Wheldon.  There 
have  naturally  been  many  reviews  and  short  discussions  of  Men- 
delian theories  and  among  them  that  of  Castle  entitled  "  Mendel's 
Laws  of  Heredity"  (Science,  vol.  18,  p.  396,  1903)  and  Profes- 
sor Bailey's  "Lecture  IV"  in  Plant  Breeding,  1904,  will  per- 
haps give  the  reader  the  clearest  and  most  concise  statements. 

The  most  striking  feature  of  Mendel's  investigations  and  those 


No.  464.]          STUDIES   ON  PLANT  CELL—  VII. 


573 


of  others,  who  have  confirmed  his  conclusions,  is  the  discovery 
in  a  number  of  animals  and  plants  that  the  germ  cells  of  the 
hybrid  may  be  pure  with  respect  to  certain  characters  of  the 
parents  which  are  crossed.  This  principle  is  not  without  excep- 
tions where  the  conditions  are  apparently  complicated  by  unusual 
factors  but  the  phenomenon  when  present  is  so  striking  as  to 
command  immediate  attention  and  call  for  an  explanation  on  a 
cytological  basis.  The  purity  of  the  germ  cells  of  hybrids  means 
in  the  words  of  Castle  that  "  the  hybrid,  whatever  its  own  char- 
acter, produces  ripe  germ  cells  which  bear  only  the  pure  char- 
acters of  one  parent  or  the  other."  Thus  if  two  forms  A  and  B 
are  crossed  the  hybrid  will  have  embodied  in  itself  the  characters 
AB,  one  of  which  however  may  lie  latent,  i.  e.,  may  not  be  visi- 
ble in  the  hybrid.  Such  a  latent  character  when  present  is 
termed  recessive  while  the  prominent  character  is  termed  domi- 
nant. In  a  simple  case  some  of  the  offspring  of  the  hybrid  AB 
will  be  found  to  have  the  character  of  A  alone,  some  of  them  of 
B  alone,  and  some  of  them  will  again  have  the  mixed  characters 
AB.  If  experiments  are  carried  out  on  an  extensive  scale  the 
proportions  of  these  offspring  from  the  hybrid  may  exhibit  the 
remarkable  fact  that  there  are  about  twice  as  many  forms  of  AB 
as  either  A  or  B,  i.  e.,  the  proportions  of  A's,  AB's,  and  B's  are 
in  the  ratio  of  i  :  2  :  i .  Furthermore  the  offspring  of  A  when 
bred  among  themselves  remain  absolutely  true  producing  a  suc- 
cession of  pure  forms  all  A's  and  the  same  results  follow  when 
the  offspring  of  B  are  closely  bred.  But  when  forms  with  the 
mixed  characters  AB  are  bred  with  one  another  their  offspring 
break  up  as  before  into  three  types  A,  AB,  and  B  in  numerical 
proportions  expressed  by  the  same  ratio  1:2:1.  The  history 
is  simply  told  in  the  following  diagram  where  the  number  of  off- 
spring is  assumed  to  be  4. 

f  i  A 4  A 1 6  A 64  A 

f    2  A 8  A 12  A 

Form  A,  f   4A i6A 

f   8A' 


Hybrid  AB<| 

I 


Form    B 


4  AB«|          8AB-|  i6AB 


8B 

L    46 i6B 

2B 8B 326 

4  B- i6B 646 


574  THE   AMERICAN  NATURALIST.        [VoL.  XXXIX. 

This  remarkable  proportion  of  forms  derived  from  the  hybrids 
AB,  i.  e.,  A,  AB,  and  B  in  the  ratio  1:2:1  can  only  be  explained 
on  the  assumption  that  the  germ  cells  of  the  hybrid  are  pure 
with  respect  to  the  characters  of  either  one  or  the  other  of  the 
parents.  The  gametes  from  the  hybrid,  with  the  pure  charac- 
ters of  either  A  or  B  and  approximately  equal  in  number,  may 
unite  with  one  another  in  three  possible  combinations  AA,  AB, 
or  BB  forming  three  types  of  offspring,  one  pure  A,  another 
mixed  AB,  and  the  last  pure  B.  By  the  law  of  chance  the  pro- 
portions of  these  combinations  ( AA,  AB,  and  BB)  in  a  simple 
case  will  be  in  the  ratio  i  :  2  :  i.  This  assumption  of  the  purity 
of  the  germ  cells  of  hybrids  has  been  found  to  conform  with  the 
facts  in  a  number  of  simple  experiments  where  two  characters 
such  as  A  and  B  were  sharply  contrasted.  When  one  of  the 
characters  in  the  hybrid  is  dominant  and  the  other  recessive  the 
ratio  can  be  expressed  as  D  :  UR :  R  as  i  :  2  :  i  which  is  merely 
a  substitution  of  D  and  R  for  the  characters  A  and  B. 

There  are  of  course  many  factors  which  tend  to  modify  the 
ratios  as  stated  above  and  complicate  the  results.  Thus  the 
normal  number  of  gametes  may  be  of  varying  vigor  and  mortal- 
ity so  that  there  will  be  proportionately  more  or  less  of  one  type 
of  fusion  than  is  called  for  by  the  law  of  chance.  Sometimes 
the  characters  of  the  parents  remain  evenly  balanced  in  the 
hybrid  and  refuse  to  split  up  in  the  succeeding  generations, 
remaining  in  a  stable  union  in  the  germ  cells  produced  by  the 
hybrid.  Such  conditions  prove  exceptions  both  to  the  law  of 
dominance  and  to  that  of  purity  of  the  germ  cells.  From  these 
exceptions  and  particularly  the  last  it  is  difficult  to  believe  that 
any  large  proportion  of  the  germ  cells  is  absolutely  pure,  i.  e., 
bearing  only  the  pure  characters  of  one  parent  or  the  other. 
H'ovvever,  there  is  much  evidence  from  our  knowledge  of  the 
distribution  of  the  chromosomes  from  one  generation  to  the  next, 
that  certain  relations  are  possible  in  the  separation  of  germ  plasm 
which  approximate  the  ratios  of  Mendel's  law  and  while  rarely 
giving  absolutely  pure  germ  cells  nevertheless  do  make  possible 
a  large  proportion  of  relatively  pure  cells. 

Let  us  examine  now  the  chromosome  history  as  a  possible 
physical  basis  for  the  Mendalian  principles.  Such  considerations 


No.  464.]  STUDIES   ON  PLANT   CELL.—  VII.  575 

must  rest  on  the  assumption  of  what  is  termed  the  individuality 
of  the  chromosome.  This  means  that  the  chromosome  is 
believed  to  be  a  permanent  organ  of  the  cell  which-neiLcr  loses 
its  organic  entity  although  the  form  may  be  frequently  obscured, 
as  in  the  resting  nucleus,  and  which  reproduces  by  fission  during 
mitosis.  We  have  given  in  other  connections  the  evidence  upon 
which  the  above  view  rests,  evidence  -accumulated  from  the 
studies  of  the  critical  periods  of  garnetogenesis,  fertilization,  and 
sporogenesis  (with  its  reduction  phenomena)  in  plants  and  of 
garnetogenesis  and  fertilization  in  animals.  All  investigations 
indicate  that  paternal  and  maternal  chromosomes  maintain  com- 
plete independence  in  the  sexually  formed  cell  or  fertilized  egg 
and  in  the  mitoses  of  cleavage  so  far  as  these  have  been  fol- 
lowed. Also,  descendants  of  the  chromosomes  which  became 
associated  with  fertilization  have  been  recognized  by  their  form 
at  the  end  of  the  life  history  during  the  reduction  phenomena  of 
garnetogenesis  in  certain  animals  (Sutton,  :  02,  :  03  ;  Montgom- 
ery, :  04)  and  of  sporogenesis  in  the  hybrids  of  Drosera  (Rosen- 
berg, :  O4a,  :O4b).  Furthermore,  the  entire  history  of  chromo- 
some reduction  in  both  animals  and  plants  finds  a  satisfactory 
explanation  only  in  the  belief  that  descendants  of  maternal  and 
paternal  chromosomes  are  distributed  as  organic  entities  by  the 
peculiar  mitoses  of  this  period.  * 

There  is  a  general  agreement  that  the  somatic  chromosomes 
of  animals  and  the  sporophytic  of  plants  become  grouped  in 
pairs  to  form  bivalent  structures  before  the  heterotypic  mitosis 
of  the  reduction  division  whether  this  be  present  in  the  primary 
gametocyte  (animals)  or  the  spore  mother-cell  (plants).  The 
bivalent  chromosomes  (pairs  of  chromosomes,  dyads)  may  be- 
come transformed  into  tetrads  before  the  heterotypic  mitosis  by 
a  division  of  each  chromosome  in  the  pair,  as  is  characteristic  of 
animals,  or  this  division  may  be  delayed  until  a  somewhat  later 
period  during  the  heterotypic  mitosis,  as  in  plants.  We  are  not 
concerned  now  with  the  dispute  as  to  how  the  pairs  of  chromo- 
somes come  to  lie  side  by  side  to  form  the  bivalent  structure  or 
how  tetrads  are  developed,  activities  which  may  indeed  be  vari- 
ous in  different  types  and  which  will  only  be  understood  by  a 
greater  body  of  observations  than  we  have  at  present  (see  dis- 


576  THE    AMERICAN  NATURALIST.       [VOL.  XXXIX. 

cussion  of  "  Reduction  of  Chromosomes ").  The  important 
point  for  us  is  the  belief  that  the  appearance  of  the  bivalent 
chromosomes  during  reduction  is  due  to  the  temporary  union  of 
somatic  or  sporophytic  chromosomes  in  pairs  and  further  that 
ths  reducing  divisions  distribute  the  members  of  the  pair,  which 
are  believed  to  be  descendants  of  the  maternal  and  paternal 
chromosomes  of  the  previous  generation,  as  organic  entities  to 
the  generation  which  is  to  follow. 

It  is  difficult  to  overestimate  the  importance  of  this  general- 
ization. If  the  program  prove  to  be  correct  as  stated  above  and 
if  the  chromosome  is  established  beyond  doubt  as  a  self-perpet- 
uating organ  of  the  cell  and  a  bearer  of  hereditary  characters 
we  have  then  the  possibility  of  studying  the  actual  manner  in 
which  these  structures  are  passed  on  from  one  generation  to  the 
next  and  perhaps  determine  the  ratios  or  combinations  through 
which  the  distribution  is  effected.  The  difficulty  of  making  an 
exact  determination  of  ratios  in  any  form  so  far  studied  lies  in 
our  inability  to  distinguish  the  chromosomes  of  maternal  and 
paternal  origin.  There  is  much  evidence  that  the  pairs  of 
somatic  and  sporophytic  elements,  which  form  the  bivalent 
chromosomes  of  the  reduction  mitoses  of  animals  and  plants 
respectively,  are  of  different  parentage  but  we  do  not  know 
whether,  or  not  there  is  any  rule  in  the  arrangement  of  the  pairs 
on  the  spindles  of  these  mitoses  although  this  is  hardly  to  be 
expected.  Cannon  (:O2,  :  O3a)  and  others  have  held  that  the 
mitoses  of  reduction  brought  about  the  complete  separation  of 
the  maternal  and  paternal  chromosomes  so  that  two  of  the 
resultant  four  nuclei  contain  chromosomes  from  one  parent  and 
two  from  the  other,  and  the  germ  cells  are  in  consequence  abso- 
lutely pure  in  character.  But  this  view  was  soon  shown  by  Sut- 
ton  (103,  p.  233;  accepted  by  Cannon,  :  O3b)  to  be  at  variance 
with  the  facts  of  breeding  for  if  germ  cells  of  hybrids  are  abso- 
lutely pure  there  could  be  no  further  change  by  cross-breeding 
and  the  first  cross  would  be  repeated  over  and  over  again  with- 
out any  divergence  from  the  type,  which  is  contrary  to  experi- 
ence and  fact.  The  pairs  of  chromosomes  are  probably  arranged 
in  every  possible  order  and  the  maternal  and  paternal  elements 
are  distributed  in  every  possible  combination  by  the  reducing 


No.  464.]  STUDIES   ON  PLANT   CELL.— VII.  577 

divisions.  If  this  is  true  then  by  the  law  of  chance  the  propor- 
tions of  germ  cells  of  the  hybrid  which  are  absolutely  pure  (con- 
taining chromosomes  entirely  from  one  parent)  woukf  be  small. 
Likewise  there  would  be  a  small  proportion  of  germ  cells  in 
which  the  paternal  and  maternal  chromosomes  are  equally  dis-. 
tributed.  And  in  contrast  to  these  two  groups  the  great  major- 
ity of  germ  cells  would  have  a  marked  preponderance  of  chromo- 
somes derived  from  one  parent  or  the  other  and  this  condition 
may  be  termed  one  of  relative  purity. 

We  shall  now  summarize  the  cytological  evidence  for  the  con- 
clusions of  the  paragraph  above,  first  with  respect  to  the  actual 
distribution  of  the  somatic  and  sporophytic  chromosomes  as 
entities  during  the  mitoses  of  reduction,  and  second  as  to  the 
probability  of  the  bivalent  chromosomes  consisting  of  a  pair  of 
maternal  and  paternal  elements.  The  evidence  on  the  first 
point  has  been  treated  as  regards  plants  in  our  own  account  of 
"  Reduction  of  the  Chromosomes  "  and  need  not  be  repeated. 
With  respect  to  the  possibilities  of  distinguishing  maternal  and 
paternal  chromosomes  throughout  a  life  history  and  especially 
at  the  period  of  chromosome  reduction  we  must  consider  briefly 
the  remarkably  favorable  studies  of  Button,  Montgomery,  Moenk- 
haus,  Baumgartner,  and  Rosenberg. 

Sutton  (:O2,  :  03)  discovered  in  the  "lubber  grasshopper" 
(Brachystola  magna)  a  form  in  which  the  somatic  chromosomes, 
23  in  number,  are  markedly  different  in  size,  presenting  a  graded 
series  with  respect  to  pairs  in  which  the  two  elements  are  ap- 
proximately equal.  There  are  then  1 1  types  of  chromosomes  in 
two  groups,  a  pair  of  each  type,  and  in  addition  an  accessory 
chromosome  which  remains  apart  from  the  rest  in  a  special 
vesicle  of  its  own.  These  two  sets  of  1 1  chromosomes  appear 
with  regularity  throughout  the  mitoses  leading  up  to  the  reduc- 
tion divisions  of  spermatogenesis.  Previous  to  the  reducing 
divisions  the  chromosomes  of  each  pair  become  closely  asso- 
ciated end  to  end  so  that  1 1  threads  appear  which  form  1 1  biva- 
lent chromosomes  (dyads)  that  later  become  tetrads  through  the 
division  of  each  chromosome  in  the  pair.  Sutton  concludes  that 
the  somatic  chromosomes  which  make  up  each  bivalent  structure 
conjugate  during  synapsis  and  that  the  transverse  fission  which 


578  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

appears  during  the  formation  of  the  tetrad  simply  separates  the 
two  somatic  chromosomes  of  the  pair,  while  the  longitudinal 
fission  is  the  usual  division  of  chromosomes,  appearing  prema- 
turely at  this  time.  The  conclusion  is  natural  that  the  two 
series  of  the  1 1  pairs  consist  of  maternal  and  paternal  chromo- 
somes which  are  distributed  as  organic  entities  by  the  reducing 
divisions.  But  there  are  no  reasons  for  supposing  that  all  of 
the  paternal  chromosomes  will  pass  into  one  set  of  germ  cells 
and  all  of  the  maternal  into  another  but  rather  that  the  ratios 
of  distribution  will  be  by  the  law  of  chance  according  to  which 
the  great  majority  of  germ  cells  will  have  a  marked  preponder- 
ance of  chromosomes  from  one  parent  or  the  other,  and  will 
therefore  be  relatively  pure.  An  exceedingly  small  proportion 
of  germ  cells  may,  by  the  law  of  chance,  contain  chromosomes 
entirely  of  maternal  or  paternal  extraction,  and  an  equally  small 
proportion  may  contain  6  chromosomes  of  one  parent  and  5  of 
the  other.  The  accessory  chromosome  divides  but  once  during 
the  mitoses  of  spermatogenesis  so  that  two  of  the  spermatozoids 
have  ii  chromosomes  and  two  12.  No  accessory  chromosome 
appears  in  the  mitoses  of  ob'genesis  indicating  that  the  female 
insect  lacks  this  structure  which  confirms  the  belief  of  McClung 
(:  02)  and  others  that  the  accessory  chromosome  is  a  determin- 
ant of  the  male  sex. 

Montgomery  in  a  series  of  studies  upon  insects  and  Amphi- 
bians, which  are  summarized  in  a  recent  paper  (:  04),  reached 
conclusions  in  striking  support  of  the  theories  of  the  individu- 
ality of  the  chromosomes,  the  association  of  pairs  of  chromo- 
somes during  synapsis  to  form  bivalent  structures  and  the  prob- 
ability of  the  elements  of  each  pair  (bivalent  chromosomes)  being 
of  maternal  and  paternal  origin  respectively.  His  results  on  the 
last  point  are  of  especial  interest  in  relation  to  hybridization. 
In  a  large  number  of  insects,  chiefly  Hemiptera,  Montgomery 
has  found  pairs  of  chromosomes,  which  he  terms  heterochromo- 
somes,  much  smaller  or  much  larger  than  the  others  and  these 
may  be  followed  through  mitosis  from  one  nucleus  to  another. 
The  heterochromosomes  of  each  pair  are  known  to  unite  with 
one  another  during  synapsis  to  form  the  bivalent  chromosomes 
of  the  reduction  mitoses  and  they  then  become  separated,  each 


No.  464.]  STUDIES   ON  PLANT  CELL.— VII.  579 

dividing  once,  so  that  every  germ  cell  receives  a  single  hetero- 
chromosome  of  whatever  sort.  Fertilization  then  brings  the 
heterochromosomes  together  again  in  pairs  until  the  Jiexl  period 
of  chromosome  reduction.  This  history  is  then  parallel  to 
Button's  account  of  the  lubber  grasshopper  (Brachystola),  the 
difference  being  that  the  latter  form  presents  a  remarkably 
graded  set  of  paired  chromosomes.  Montgomery  regards  the 
small  chromosomes  and  the  accessory  chromosome  as  structures 
tending  to  disappear  in  a  process  of  evolution  from  a  higher 
chromosomal  number  to  a  lower. 

Moenkhaus  (:  04)  crossed  reciprocally  two,  species  of  fishes 
(Fnndulus  Jieteroclitus  and  Menidia  no  tat  a}  and  obtained  hybrid 
embryos  which  reached  an  advanced  stage  of  development. 
The  chromosomes  of  the  parents  are  readily  distinguished  by 
size  and  form.  These  chromosomes  were  followed  throughout 
the  development  of  the  hybrid  embryo  and  were  found  to  retain 
their  peculiarities  so  that  the  two  sets  may  be  easily  separated 
in  favorable  tissues.  This  investigation  furnishes  some  of  the 
strongest  evidence  of  the  individuality  of  the  chromosome  and 
the  complete  independence  throughout  the  life  history  of  the 
two  sets  derived  from  each  parent.  Could  these  hybrid  embryos 
be  raised  to  maturity  we  should  expect  to  find  during  spermato- 
genesis  and  oogenesis  an  association  of  the  chromosomes  in 
pairs,  those  of  paternal  extraction  with  those  of  maternal  to 
form  the  bivalent  chromosomes  preliminary  to  the  reducing  divi- 
sions, and  a  distribution  to  the  sexual  cells  in  varying  propor- 
tions which  would,  however,  give  a  very  large  ratio  of  relatively 
pure  germ  cells. 

Baumgartner  (:  04)  in  studies  upon  spermatogenesis  in  the 
cricket  (Gryllus)  was  able  to  distinguish  the  chromosomes  by 
their  form,  following  them  through  the  mitoses  of  reduction. 
Most  of  the  chromosomes  have  the  form  of  straight  or  bent  rods 
but  there  are  apparently  two  rings  in  each  set  in  G.  domesticus. 
The  variation  in  the  form  of  chromosomes  in  the  nucleus  is  well 
known  but  it  has  not  been  supposed  that  a  definite  form  might 
be  characteristic  of  an  element  and  be  maintained  throughout 
the  successive  mitoses  of  a  life  history  as  seems  probable  from 
Baumgartner's  results. 


580  THE  AMERICAN  NATURALIST.        [VOL.  XXXIX. 

Rosenberg's  (:  04.3.,  :  O4b)  studies  on  hybrids  of  Drosera  rotun- 
difolia  (with  ten  chromosomes  in  the  gametophyte)  and  D.  longi- 
folia  (with  twenty  chromosomes)  offer  clear  evidence  that  the 
chromosomes  which  unite  in  pairs  to  form  bivalent  structures 
preliminary  to  the  reduction  phenomena  of  sporogenesis  are  of 
different  parentage.  The  sporophyte  number  of  chromosomes 
in  the  hybrid  is  thirty,  as  would  be  expected.  The  reduced 
number  appearing  at  the  first  mitosis  of  sporogenesis  is,  however, 
not  fifteen  but  twenty  chromosomes,  ten  of  which  are  plainly 
double  the  size  of  the  other  ten.  The  explanation  of  this  inter- 
esting condition  is  that  the  ten  chromosomes  of  D.  rotnndifolia 
unite  with  one  half  of  the  twenty  chromosomes  of  D.  longifolia 
giving  ten  large  bivalent  structures  accompanied  by  the  ten 
chromosomes  of  D.  longifolia  which  are  without  mates.  This 
explanation  finds  clear  support  in  the  facts  that  the  chromo- 
somes of  D.  rotnndifolia  are  larger  than  those  of  D.  longifolia 
and  that  the  bivalent. structure  consists  of  a  larger  and  a  smaller 
element  thus  giving  clear  evidence  that  the  pairs  of  chromosomes 
which  unite  in  Drosera  are  of  different  parentage.  The  single 
chromosomes  which  are  without  mates  may  pass  to  one  or  the 
other  of  the  poles  of  the  spindle  or  may  be  left  behind  when  the 
daughter  nuclei  are  formed. 

This  group  of  investigations  illustrates  very  clearly  the  charac- 
ter of  the  evidence  that  is  leading  many  biologists  to  assign  to 
the  chromosomes  the  functions  of  bearing  and  distributing  hered- 
itary characters.  The  question  at  once  comes  up  as  to  whether 
or  not  the  chromosomes  may  differ  among  themselves  to  a 
greater  or  less  extent  even  in  the  same  species  or  individual. 
Montgomery,  Sutton,  with  others,  have  established  a  difference 
in  the  size  of  chromosomes.  Baumgartner  distinguishes  differ- 
ences inform  in  the  same  species  and  the  studies  of  Moenkhaus 
and  Rosenberg  have  shown  that  the  chromosomes  of  different 
parents  may  retain  their  peculiarities  of  form  in  hybrids  and  be 
really  separated.  To  these  investigations  should  be  added  the 
recent  conclusions  of  Boveri  ( :  02,  :  04),  that  chromosomes  actu- 
ally differ  in  function.  Boveri  found  that  the  chromosomes  of 
eggs  of  echinoderms  that  were  fertilized  by  two  or  more  sperms 
are  distributed  by  multipolar  spindles  to  a  varying  number  of 


No.  464.]  STUDIES   ON  PLANT  CELL.— VII.  581 

blastomeres  which  in  consequence  received  a  varying  number 
and  assortment  of  chromosomes.  Boveri  then  separated  these 
blastomeres  and  followed  their  independent  development  into 
larval  stages  which  exhibited  marked  differences  in  form  that 
could  be  correlated  with  the  irregularities  in  the  number  of 
chromosomes  contained  in  each,  thus  suggesting  that  specific 
chromosomes  have  specific  functions.  With  this  sort  of  evi- 
dence accumulating  from  both  the  morphological  and  physio- 
logical side  it  is  not  surprising  that  many  biologists  believe 
that  specific  characters  are  actually  held  or  are  controlled  by 
chromosomes  or  groups  of  chromosomes. 

Such  views  of  course  presuppose  that  the  chromosomes  retain 
a  high  degree  of  independence  of  one  another  and  that  variation 
is  expressed  chiefly  through  different  combinations  of  chromo- 
somes and  not  by  modifications  of  the  chromosomes  themselves. 
Yet  there  is  strong  evidence  of  an  actual  mixing  or  interchange 
of  the  idioplasm  among  the  chromosomes.  This  possibility 
which  is  of  course  contradictory  to  the  view  of  the  complete 
independence  of  the  chromosomes  finds  its  chief  support  in  the 
close  association  of  the  pairs  of  chromosomes  with  the  organiza- 
tion of  the  reduced  number  of  bivalent  structures  during  synap- 
sis.  These  pairs  have  been  reported  so  intimately  united  as  to 
be  actually  fused.  Allen  (:O5)  has  described  for  Lilium  the 
union  of  two  sets  of  chromomeres,  one  believed  to  be  derived 
from  a  paternal  spirem  and  the  other  from  a  maternal,  which 
come  to  lie  side  by  side  during  synapsis  and  unite  to  form  a 
spirem  with  a  single  series  of  fusion  chromomeres.  This  single 
(fusion)  spirem  later  splits  longitudinally  and  the  two  halves  are 
regarded  as  again  representing  maternal  and  paternal  spirems 
but  there  are  evidently  opportunities  during  the  period  of  fusion 
for  significant  reciprocal  interaction  between  the  two  idioplasms. 
This  conception  of  the  fusion  of  idioplasm  from  the  two/ parents 
is  an  old  view  which  has  been  held  by  such  well  known  biologists 
as  Hertwig  and  Strasburger. 

De  Vries  (:  03)  has  recently  discussed  the  significance  of  the 
pairing  of  chromosomes  before  the  heterotypic  mitosis  in  relation 
to  the  theory  of  pangenesis.  He  conceives  the  paternal  and 
maternal  chromosomes  as  coming  together  during  synapsis  in 


582  THE  AMERICAN  NATURALIST.      [VOL.  XXXIX. 

homologous  pairs  so  that  corresponding  pangenes  or  groups  of 
pangenes  are  brought  together  and  that  there  may  be  a  mutual 
interchange  or  transfer  of  idioplasm  with  the  result  that  the 
chromosomes  after  separating  may  contain  a  mixed  set  of  pan- 
genes  although  each  is  supposed  to  have  a  complete  assortment. 
The  interchange  makes  possible  all  forms  of  combinations  of  the 
pangenes  in  the  two  sets,  according  to  the  laws  of  chance, 
which  might  be  expressed  in  proportions  that  would  approximate 
in  some  cases  the  ratios  of  Mendel.  If  the  parents  are  widely 
different  from  one  another  their  idioplasm  may  not  correspond 
sufficiently  to  make  possible  this  union  and  interchange  of 
pangenes  so  that  the  process  is  suppressed  and  the  hybrid  is 
sterile. 

Allen  (:O5,  p.  247)  points  out  that  the  union  of  two  spirems 
during  synapsis  with  the  fusion  of  two  sets  of  chromomeres, 
according  to  his  account  of  the  lily,  offers  a  number  of  possibil- 
ities with  respect  to  the  constitution  of  idioplasm  following  the 
reduction  mitosis,  (i)  There  may  be  such  a  fusion  of  elemen- 
tary units  that  a  single  idioplasm  is  formed  different  from  either 
parent  which  would  of  course  be  distributed  equally  to  the 
reproductive  cells  by  the  subsequent  double  longitudinal  fission 
of  the  single  (fusion)  spirem.  This  would  be  expected  to  give 
hybrids  of  much  the  same  form  in  every  instance  and  these 
would  remain  stable  (constant).  (2)  There  may  be  a  greater  or 
less  mixing  or  modification  of  units  but  without  the  actual  union 
and  formation  of  a  new  idioplasm  in  the  hybrid.  Then  by  the 
splitting  of  the  single  (fusion)  spirem  there  might  result  a  dis- 
tribution of  the  mixed  idioplasm  following  ratios  or  proportions 
approximating  Mendel's  law.  (3)  There  may  be  in  part  a  fusion 
and  in  part  a  mixing  of  idioplasm  which  would  be  expected  to 
result  in  a  .varied  combination  of  parental  characters  in  the  off- 
spring. (4)  While  the  chromosomes  may  be  distributed  accord- 
ing to  ratios  similar  to  Mendel's  principles  their  respective 
characters  may  be  greatly  modified  by  their  temporary  union 
during  synapsis.  (5)  Portions  of  the  idioplasm  may  interact 
upon  one  another  so  that  when  they  are  separated  by  the  reduc- 
tion mitoses  their  character  has  become  variously  modified.  (6) 
Finally,  Allen,  of  course,  recognizes  the  possibility  that  parental 


No.  464.]  STUDIES   ON  PLANT  CELL.—  VII.  583 

idioplasm  may  be  separated  so  purely  by  the  longitudinal  split- 
ting of  the  single  (fusion)  spirem  or  through  the  distribution  of 
unmodified  sporophytic  or  somatic  chromosomes  as~to-give  abso- 
lutely and  relatively  pure  germ  cells  through  Mendelian  laws. 

Allen's  discussion,  very  briefly  summarized  above,  is  impor- 
tant for  the  emphasis  which  is  laid  upon  the  significance  of  a 
possible  mixing  of  the  parental  idioplasms  in  the  more  or  less 
complete  union  of  chromatic  material,  which  is  generally  recog- 
nized as  characteristic  of  synapsis.  There  is  a  general  tendency 
to  rest  content  when  the  chromosomes  are  accounted  for  as 
units  while  they  are  merely  the  grosser  form  of  expression  of 
the  idioplasm  whose  final  architecture  is  intricate  far  beyond  our 
present  powers  of  analysis.  Allen's  own  studies  upon  the  events 
of  synapsis  in  the  lily  with  the  regular  fusion  in  pairs  of  chromo- 
meres  of  different  parentage  may  well  cause  one  to  hesitate  in  a 
full  acceptance  of  the  chromosome  as  fixed  and  unchanged  in  its 
organic  constitution  throughout  the  life  history.  The  phenome- 
non of  hybridization  is  far  too  complex  to  be  explained  in  terms 
of  simple  ratios  and  while  some  characters  may  be  paired  or 
correlated  in  proportions  that  can  be  expressed  by  mathematical 
formulae  there  is  little  probability  that  the  assemblage  of  charac- 
ters which  make  the  species  can  be  so  definitely  grouped  as  the 
strongest  disciples  of  Mendel  may  hope.  However,  a  great 
forward  step  has  been  taken  and  we  may  expect  important 
results  from  the  empirical  methods  so  clearly  defined  by  Mendel 
and  by  the  close  investigation  that  cytologists  are  making 
of  the  history  of  idioplasmic  structures  (chromosomes)  during 
ontogeny. 

8.     XENIA. 

Xenia  is  the  "  immediate  or  direct  effect  of  pollen  on  the 
character  of  seeds  and  fruits."  The  term  was  first  proposed  by 
Focke,  in  1881,  and  is  now  well  established.  Xenia  has  long 
been  known  to  the  plant  breeder  as  one  of  the  most  interesting 
and  puzzling  problems  of  hybridization.  The  botanist  has  nat- 
urally looked  for  the  results  of  hybridization  in  the  development 
of  the  embryo  from  the  seed  since  this  structure  has  received 


584  THE   AMERICAN  NATURALIST.       [V<>L.  XXXIX. 

the  substance  of  the  sperm  nucleus  of  the  male  parent.  But 
facts  have  clearly  shown  that  the  pollen  may  also  affect  the 
structure  of  the  endosperm  in  the  seed  as  well  as  cause  the 
development  of  the  embryo.  Since  the  endosperm  holds  no 
genetic  relation  to  the  embryo  it  has  seemed  very  remarkable 
that  it  should  take  on  hybrid  qualities.  It  has  also  been  claimed 
that  other  regions  of  the  seed  or  fruit,  such  as  portions  of  the 
pericarp  were  also  affected,  but  it  is  doubtful  whether  this  is 
really  so  or  at  least  whether  such  changes  are  truly  a  feature  of 
the  protoplasmic  structure  and  thus  deeply  seated  in  the  organ- 
ism as  a  feature  of  hybridization. 

It  is  only  within  recent  years  that  a  satisfactory  theory  has 
been  suggested  for  the  influence  of  pollen  outside  of  the  embryo. 
And  this  explanation  rests  on  the  discovery  of  the  activities  of 
the  second  sperm  nucleus  which  enters  the  embryo-sac  and  which 
is  known  in  some  cases  to  unite  with  the  polar  nuclei  constitut- 
ing a  triple  nuclear  fusion  within  the  sac  that  is  generally  known 
as  "double  fertilization."  We  have  briefly  referred  to  the  phe- 
nomenon in  the  latter  part  of  the  account  of  "  Asexual  Cell 
Unions  and  Nuclear  Fusions"  in  Section  IV  and  shall  take  it 
up  now  in  greater  detail.  The  best  account  of  xenia  is  a  very 
clear  treatment  by  Webber,  in  1900. 

The  explanation  of  xenia  upon  the  facts  of  "double  fertiliza- 
tion "  was  proposed  almost  simultaneously  by  De  Vries  ('99, 
:oo),  Correns  ('99b),  and  \Vebber  (:oo).  Double  fertilization 
was  first  observed  by  Nawaschin  ('98)  in  Lilium  and  Fritillaria 
and  shortly  after  was  described  in  greater  detail  by  Guignard 
('99b)  in  other  species  of  the  same  genera  and  in  Endymion. 
Since  these  discoveries  the  phenomenon  has  been  reported  by  a 
number  of  investigators  in  many  other  forms  representing  widely 
divergent  groups  in  the  Monocotyledons  and  Dicotyledonae  and 
there  is  every  reason  to  believe  that  it  is  widespread  in  the  angio- 
sperms.  A  review  of  the  recent  literature  is  given  by  Coulter 
and  Chamberlain  (Morphology  of  the  Angiosperms,  1903,  p.  156). 
There  is  no  fixed  order  in  the  events  of  the  triple  nuclear  fusion 
of  "double  fertilization."  The  polar  nuclei  may  have  united  at 
the  time  when  the  pollen  tube  enters  the  embryo-sac,  in  which 
case  the  second  sperm  nucleus  coalesces  with  an  organized  fusion 


No.  464.]  STUDIES   ON  PLANT  CELL.— VII.  585 

endosperm  nucleus.  Or,  the  two  polar  nuclei  and  the  sperm 
nucleus  may  all  three  fuse  together  practically  simultaneously. 
And  again  the  sperm  nucleus  may  unite  first  with  o_ne_of  the 
polar  nuclei  and  the  second  be  drawn  later  into  the  triple  fusion. 
But  no  cases  seem  to  have  been  reported  in  which  but  one  polar 
nucleus  unites  with  the  sperm  leaving  the  other  free  although 
such  a  combination  may  be  expected.  Also,  no  one  has  ob- 
served an  independent  division  of  the  sperm  nucleus  within  the 
endosperm,  although  as  we  shall  see,  there  are  reasons  for  believ- 
ing that  such  a  development  may  sometimes  take  place. 

We  have  already  given  in  Section  IV  the  reason  why  these 
triple  nuclear  fusions  may  be  kept  apart  from  sexual  phenomena 
since  we  have  no  knowledge  of  the  phylogenetic  history  of  the 
processes  involved.  It  seems  best  at  least  for  the  present  to 
regard  the  phenomenon  as  a  special  development  associated  with 
the  peculiar  and  highly  specialized  conditions  within  the  embryo- 
sac.  This  detailed  and  highly  difficult  problem  of  phylogeny  has 
no  especial  bearing  on  the  physiological  features  of  xenia  with 
which  we  are  at  present  concerned. 

The  best  understood  examples  of  xenia  are  found  in  the 
hybrids  of  maize  and  are  clearly  described  in  the  very  interest- 
ing paper  of  Webber  (:oo).  As  is  well  known,  some  of  the 
varieties  of  corn  are  distinguished  among  other  characters  by 
the  color  of  the  kernels,  which  are  blue,  red,  yellow,  and  white, 
and  also  by  the  surface,  which  is  smooth  in  the  starchy  corns 
(flint  or  dent)  and  wrinkled  in  the  sugary  sweet  corns.  When 
well  marked  pure  races  are  grown  out  of  reach  of  chance  cross- 
pollination,  the  offspring  remain  true  to  their  seed  characters 
but  it  has  long  been  known  that  the  varieties  of  corn  hybridize 
very  readily  so  that  when  grown  close  together  the  ears  will  very 
frequently  present  seeds  mixed  as  to  color  and  texture.  Thus 
when  exposed  to  cross-pollination  a  corn  which  is  characteris- 
tically yellow  or  white  may  bear  blue  or  red  kernels  or  a  form 
with  wrinkled  and  starchy  kernels  may  develop  smooth  starchy 
corn  if  varieties  with  these  characters  are  in  the  vicinity.  The 
color  character  is  known  to  lie  in  these  examples  in  the  outer 
layer  of  the  endosperm  (aleurone  layer)  and  of  course  the  food 
material  whether  prevailingly  starch  or  sugar,  which  gives  the 


586  THE  AMERICAN  NATURALIST.      [VOL.  XXXIX. 

surface  a  texture  smooth  or  wrinkled,  is  stored  within  the  endo- 
sperm. 

The  clearness  of  xenia  in  the  maize  has  led  to  a  number  of 
careful  studies  on  cross-pollination  beginning  with  the  work  of 
Vilmorin  (1866),  Hildebrand  (1867),  and  Friedrich  Kornicke 
(1872).  The  possible  explanation  of  xenia  in  maize  through 
"double  fertilization"  which  introduces  qualities  of  the  male 
parent  from  the  pollen  into  the  endosperm  was  suggested  by 
experiments  of  De  Vries  on  hybridizing  maize  in  the  summers 
of  1898-99  and  Correns  and  Webber  in  1899.  De  Vries  ('99, 
:  oo)  pollinated  a  wrinkled-seeded  sugar  corn  from  a  variety  of 
smooth  starchy  corn  and  obtained  smooth  starchy  kernels  which 
when  cultivated  in  the  succeeding  summer  were  found  to  be  true 
hybrids.  He  concluded  that  this  furnished  experimental  proof 
that  the  endosperm  of  the  sugar  corn  was  affected  by  the 
entrance  of  a  sperm  nucleus  from  the  starchy  variety  according 
to  the  theory  of  "double  fertilization  "  proposed  by  Nawaschin 
('98). 

Correns  ('99b)  in  the  same  year  expressed  similar  conclusions 
in  a  clear  statement  of  the  theoretical  aspects  of  the  problem  of 
xenia  as  found  in  Zea  mays.  Correns  advanced  a  number  of 
propositions  some  of  which  should  be  noted  for  their  speculative 
interest.  Thus  he  states  (proposition  7)  that  the  influence  of 
the  new  pollen  (i.  e.,  from  the  male  parent  of  the  hybrid)  is 
expressed  as  xenia  only  in  the  endosperm  and  (proposition  8) 
only  in  the  pigment  present  or  the  chemical  nature  of  the  reserve 
material  whether  starchy  or  sugary.  If  the  two  races  differ 
only  in  the  presence  of  one  character,  as  in  the  color  of  the 
aleurone  layer,  that  character  is  only  found  in  xenia  when 
brought  by  the  pollen  (proposition  10).  Xenia  is  then  only 
expressed  in  a  hybrid  (proposition  14)  by  the  formation  of  a  pig- 
ment which  the  race  of  the  female  parent  does  not  possess  or  of 
a  more  complicated  chemical  compound  (such  as  starch)  in  place 
of  a  simpler  (as  dextrin).  Correns  (:  01)  later  presented  in  a 
lengthy  paper,  beautifully  illustrated,  the  full  results  of  his 
studies  on  xenia  in  maize  with  a  discussion  of  the  hybrids. 

Webber  (:oo)  also  simultaneously  with  De  Vries  and  Correns 
conducted  extensive  experiments  in  hybridizing  a  number  of 


No.  464.]  STUDIES   ON  PLANT  CELL.—  VII.  587 

varieties  of  corn  distinguished  by  the  color  of  the  kernels,  which 
were  white,  yellow,  red,  or  blue  and  by  the  texture  whether 
smooth,  hard,  and  starchy  (dent  or  flint  corn)  or  wrinkled  and 
sugary  (sweet  corn).  The  results  of  his  investigation  are  admir- 
ably presented  with  excellent  illustrations.  He  found  that  the 
smooth  kernel  and  starchy  endosperm  of  the  dent  and  flint  corn 
were  transmitted  very  conspicuously  as  xenia  when  these  forms 
were  employed  as  the  male  in  crossing  with  the  sweet  corns 
whose  kernels  are  wrinkled  and  sugary.  The  characters  of  the 
sweet  corns  do  not  seem  to  be  expressed  as  xenia  when  smooth, 
starchy,  dent  corn  is  used  as  the  female  member  of  the  hybrid. 
This  experiment  would  seem  to  support  Correns'  proposition 
number  14  that  a  more  complicated  compound  is  always  formed 
in  xenia  in  place  of  a  less  complex.  But  Webber  found  that 
flint  corn,  which  is  smooth  and  starchy,  when  pollinated  with 
a  form  of  sweet  corn  developed  the  wrinkled  kernel  and  sugary 
type  of  endosperm  of  the  male  member  indicating  that  this  rule 
of  Correns  is  not  universal.  And  McClure  ('92)  obtained  simi- 
lar results  in  crossing  a  white  dent  race  with  pollen  of  Black 
Mexican  which  is  a  sugar  corn  with  black  kernels.  The  product 
in  this  case  showed  xenia  clearly  in  having  the  wrinkled  blue- 
black  kernels  of  the  male  sugar  corn. 

Some  of  Webber's  most  striking  results  were  obtained  in  pol- 
linating yellow  and  white  corns  with  blue-black  and  red  races. 
The  color  was  transmitted  as  xenia  in  a  most  striking  manner. 
Webber  agrees  with  other  authors  that  the  color  is  only  present 
in  the  endosperm  of  the  kernels.  Thus  the  red  of  certain  dent 
corn,  which  lies  in  the  pericarp,  is  not  passed  on  as  xenia  and 
McClure  observed  the  same  facts  in  experiments  with  cranberry 
corn  whose  color  lies  in  the  seed  coat  and  is  not  transmitted 
when  employed  as  the  male  member  in  crossing  with  white 
corns.  Webber's  experiments  show,  as  do  those  of  other  inves- 
tigators, that  the  absence  of  color  in  the  kernels  of  the  male 
parent  does  not  seem  to  affect  the  tint  of  the  kernels  when  the 
female  is  markedly  colored,  in  agreement  with  Correns'  proposi- 
tion number  10.  But  Webber  is  not  convinced  that  some 
influence  might  not  be  exerted  on  colored  corn  when  pollinated 
from  races  with  colorless  endosperm,  because  of  certain  experi- 
ments on  variegated  xenia  which  will  be  described  presently. 


588  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

These  experiments  of  De  Vries,  Correns,  Webber,  and  others 
have  established  experimentally  the  facts  of  xenia  and  Nawas- 
chin's  theory  of  double  fertilization  seems  to  offer  the  only 
explanation  of  the  phenomenon.  But  it  was  left  to  Guignard 
(:oi)  to  make  the  concluding  observation  that  a  second  sperm 
nucleus  does  actually  enter  into  the  composition  of  the  endo- 
sperm of  maize,  and  this  fact  clinched  the  argument  which  up 
to  this  time  had  been  a  speculation. 

Webber  has  made  a  very  important  addition  to  the  theory  of 
"  double  fertilization  "  as  an  explanation  of  xenia  in  some  obser- 
vations and  speculations  on  a  mottled  condition  which  is  some- 
times present  when  white  corns  are  pollinated  by  colored.  He 
found  that  the  color  was  sometimes  only  transmitted  in  spots  as 
when  Hickory  King  was  pollinated  by  Cuzco,  or  perhaps  only 
half  a  kernel  may  be  colored.  Webber  offers  the  hypothesis 
that  the  second  sperm  nucleus  may  enter  the  embryo-sac  but 
instead  of  uniting  with  the  two  polar  nuclei  to  form  a  triple 
fusion  may  itself  divide  separately  and  thus  gives  rise  to  a 
progeny  very  different  from  the  other  endosperm  nuclei. 
There  might  then  be  two  sets  of  nuclei  in  the  endosperm  one  of 
which  is  composed  of  nuclei  which  would  come  directly  from 
the  male  parent.  These  latter  then  might  become  distributed 
throughout  the  embryo-sac  but  would  tend  to  remain  in  groups 
as  multiplication  progressed  and  would  certainly  be  expected  to 
influence  the  character  of  the  tissue  which  is  formed  later  when 
the  walls  are  developed  around  the  free  nuclei.  As  Webber 
expresses  it,  there  might  be  formed  islands  of  tissue  in  the 
endosperm  whose  cells  contain  nuclei  derived  directly  from  the 
second  sperm  and  such  tissue  would  be  expected  to  show  char- 
acters of  the  male  parent  in  spots  as  xenia.  Again,  if  the  sperm 
nucleus  should  unite  with  only  one  of  the  polar  nuclei  and  the 
other  should  give  rise  to  an  independent  progeny  we  should 
expect  similar  mixed  conditions  in  the  endosperm,  with  xenia 
only  expressed  in  the  areas  dominated  by  nuclei  containing 
material  derived  from  the  sperm. 

There  have  been  reported  illustrations  of  xenia  in  tissues  out- 
side of  the  endosperm  but  we  are  fully  justified  in  awaiting 
their  confirmation  before  accepting  them,  especially  since  some 


No.  464.]  STUDIES   OF  PLANT  CELL— VII.  589 

have  failed  to  stand  the  test  of  critical  investigation,  in  the 
light  of  the  present  theory.  Thus  certain  investigators  have 
reported  xenia  in  the  color  of  the  seed  coats  of  certain  peas. 
But  Giltay  ('93)  in  a  series  of  experiments  found  no  instance 
where  color  was  transmitted  to  these  tissues.  The  pigments  in 
these  plants  lie  in  the  cotyledons  of  the  embryo  which  of  course 
are  readily  visible  through  the  thin  coats  of  the  seed.  While 
the  present  theory  of  xenia  is  very  recent  and  has  been  critic- 
ally applied  in  few  forms,  it  seems  thoroughly  satisfactory  in 
every  particular  with  no  clearly  established  evidence  against  it. 


LITERATURE    CITED    IN    SECTION    V,  "THE    PLANT 

CELL." 

ALLEN. 

:  04.     Chromosome    Reduction  in  Lilium  canadense.     Bot.  Gaz.,  vol.  37, 

p.  464. 
ALLEN. 

:05.     Nuclear  Division  in  the  Pollen  Mother-Cells  of  Lilium  canadense. 

Annals  of  Bot.,  vol.  19,  p.  189. 
ATKINSON. 

'99.     Studies  on  Reduction  in  Plants.     Bot.  Gaz.,  vol.  29,  p.  i. 
BAUMGARTNER. 

:04.     Some   New   Evidence   for  the   Individuality  of  the  Chromosomes. 

Biol.  Bull.,  vol.  8,  p.  i . 
BELAJEFF. 

'98.     Ueber  die    Reductionstheilung  des    Pflanzenkernes.     Ber.  d.  deut. 

hot.  Gesellsch.,  vol.  16,  p.  27. 
BEARD. 

'95.     On  the  Phenomena  of  Reproduction  in  Animals  and  Plants.    Anti- 
thetic Alternation  of  Generations.     Annals  of  Bot.,  vol.  9,  p.  441. 
BERGHS. 

:  04a.     Depuis  le   spirem  jusqu'aux   chromosomes   murs  dans  la  micro- 
sporoge"nese  d  ^  A  Ilium  fistulosum  et  de  Lilium  lancifolium  (speci- 
osuin).     La  Cellule,  vol.  21,  p.  173. 
BERGHS. 

:  04b.     Depuis  la  sporogonie    jusqu'au  spireme   de'fmitif  dans  la  micro- 
sporogdnese  de  V A  Ilium  fistulosum.     La  Cellule,  vol.  21,  p.  383. 


590  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

BERGHS. 

:  05.      La   microsporoge'ne-se   de    Convallaria  maialis.     La    Cellule,   vol. 

22,  p.  43. 
BITTER. 

:04.      Parthenogenesis  und   Variabilitat  der  Bryonia    dioica.     Abh.  nat. 

Ver.  Brem.,  vol.  18,  p.  99. 
BLACKMAN. 

:  04a.     On    the    Fertilization,    Alternation  of   Generations,  and    General 

Cytology  of  the  Uredineae.     Annals  of  Bot.,  vol.  18,  p.  323. 
BLACKMAN. 

:  04b.     On  the  Relation  of  Fertilization  to  "  Apogamy  "  and  "  Partheno- 
genesis."    New  Phytologist,  vol.  3,  p.  149. 
BOVERI. 

:  02.     Ueber  mehrpolige  Mitosen   als  Mittel  zur  Analyse  des  Zellkerns. 

Verh.  d.  phys.-med.   Gesellsch.  Wiirzburg.,  vol.  35. 
BOVERI. 

:  O4.     Ergebnisse  iiber  die   Konstitution  der  chromatischen  Substanz  des 

Zellkerns.     Jena,  1904. 
BOWER. 

'86.      On  Apospory  in   Ferns.    Jour.  Linn.  Soc.  London,  Bot.,vo\.  21,  p. 

360. 
BOWER. 

'87.     On  Apospory  and   Allied    Phenomena.      Trans.  Linn.  Soc.  London, 

Bot.,  II,  vol.  2,  p.  301 . 
BOWER. 
'88.     On  some  Normal  and  Abnormal  Developments  of  the  Oophyte  in 

Trichomanes.     Annals  of  Bot.,  vol.  i,  p.  269. 
BRIZI. 
'92.     Apunti    di    teratologia    briologica.     Ann.  d.   Instit.  Bot.  d.  Roma, 

vol.  5,  p.  53. 
CALKINS. 
'97.     Chromatin  Reduction  and  Tetrad-formation  in  Pteridophytes.  Bull. 

Torrey  Bot.  Club,  vol.  24,  p.  101. 
CALKINS. 

:01.     The  Protozoa.     New  York,  1901. 
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CANNON. 

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592  THE  AMERICAN  NATURALIST.         [VOL.  XXXIX. 

DlXON. 

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FARMER  AND  MOORE. 

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GUIGNARD. 

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594  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

GUIGNARD. 

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GUIGNARD. 

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LOTSY. 

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No.  464.]  STUDIES   ON  PLANT  CELL.— VII.  595 

LOTSY. 

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LOTSY. 

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LOTSY. 

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LYON. 

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McCLUNG. 

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McCLURE. 

'92.     Corn  Crossing.     ///.  Agric.  E.vp.  Sta.  Bull.  21. 

MOENKHAUS. 

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MONTGOMERY. 

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MOORE,  A.  C. 

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MOTTIER. 

'97.     Beitrage  zur  Kenntniss  der  Kerntheilung  in  den  Pollenmutterzellen 
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MOTTIER. 

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MURBECK. 

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596  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

MURBECK. 

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No.  464.]  STUDIES   OF  PLANT  CELL —  VII.  597 

ROSENBERG. 

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ROSENBERG. 

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SCHREINER  AND  SCHREINER. 

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598  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

STRASBUKGER. 

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STRASBURGER. 

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STRASBURGER. 

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STRASBURGER. 

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magna.     Biol.  Bull.,  vol.  4,  p.  24. 
SUTTOX. 

:  03.     The  Chromosomes  in  Heredity.     Biol.  Bull.,  vol.  4,  p.  231. 
TRETJAKOW. 

'95.     Die   Betheiligung  der  Antipoden  in  Fallen  der  Polyembryonie  bei 

A  Ilium  odoruin  L.     Ber.  d.  deul.  hot.  Gesellsch.,  vol.  13,  p.  13. 
TREUB. 

'98.     L'organe  femelle  et  1'apogamie  du  Belanophora  elongata  Bl.    Ann. 
Jard.  Bot.  Buiten.,  vol.  15,  p.  i. 


No.  464.]  STUDIES   OF  PLANT   CELL.—  VII.  599 

TREUB. 

:  02.     L'organe  femelle  et  Pembryogdnese  dans  le  Ficus  hirta  Vahl.  Ann. 

Jard.  Bot.  Buiten.,  ser.  2,  vol.  3,  p.  124. 
TROW. 

-.04.     On  Fertilization  in  the  Saprolegnieae.     Annals  of  Bo/.,  vol.  18,  p. 

541- 
WEBBER. 

:00.     Xenia,  or  the  Immediate  Effect  of  Pollen  in    Maize.      U.  S.  Dept. 

Agric.,  Div.  Veg.  Path.  Phys.,  Bull.  22. 
WILLIAMS. 

:  04a.     Studies   in  the    Dictyotaceae.      I.     The   Cytology  of    the    Tetra- 
sporangium   and  the  Germinating  Tetraspore.     Annals  of  Bot., 
vol.  1 8,  p.  141. 
WILLIAMS. 

:  (Hb.     Studies  in  the  Dictyotaceas.      II.  The  Cytology  of  the  Gameto- 

phyte  Generation.     Annals  of  Bot.,  vol.  18,  p.  183. 
WILSON. 

:  00.     The  Cell  in  Development  and  Inheritance.     New  York,  1900. 
WIMWARTER. 

:  00.     Recherches    sur    I'ovoge'nese   et   I'organoge'nese    de   1'ovaire    des 

mammiferes  (lapin  et  homme).     Arch.d.  Biol.,  vol.  17,  p.  33. 
WINKLER. 

:  01.     Ueber  Merogonie   und    Befruchtung.    Jahrb.f.  wiss.  Bot.,  vol.  36, 

P-  753- 
WINKLER. 

:  O4.     Ueber  Parthenogenesis    bei    Wikstrcemia  indica  (L.)  C.  A.  Mey. 

Ber.  d.  dent.  hot.  Gesellsch.,  vol.  22,  p.  573. 
WOLFE. 

:04.     Cytological    Studies    on    Nemalion.      Annals    of  Bot.,\o\.  18,  p. 
607. 


ar«  iff1 


STUDIES    ON    THE   PLANT    CELL.—  VTIL1 

BRADLEY   MOORE    DAVIS. 

SECTION  VI.     COMPARATIVE    MORPHOLOGY  AND    PHYSIOLOGY 
OF  THE  PLANT  CELL. 

WE  shall  devote  this  section  to  the  discussion  of  a  number  of 
topics  some  of  which  have  received  brief  mention  in  the  pre- 
ceding papers  of  the  series  but  with  other  subjects  will  now 
be  considered  in  some  detail.  The  material  will  be  treated  un- 
der the  following  five  headings  :  — 

1.  The  simplest  types  of  plant  cells. 

2.  Comparisons  of  the  structures  of  some  higher  types  of 
plant  cell  with  simpler  conditions. 

3.  Some  apparent  tendencies  in  the  evolution  of  mitotic  phe- 
nomena. 

4.  The  essential  structures  of  the  plant  cell   and  their  be- 
havior in  ontogeny. 

5.  The   balance  of  nuclear  and  cytoplasmic  activities  in  the 
plant  cell. 

i.    THE  SIMPLEST  TYPES  OF  PLANT  CELLS. 

There  are  three  groups  of  plants  which  are  conspicuous  for 
the  simplicity  of  their  cell  structure.  They,  are  :  the  Cyano- 
phyceae  (blue-green  algae),  Schizomycetes  (bacteria),  and  the 
Saccharomycetes  (yeasts).  All  three  groups  have  received 
much  attention  and  there  has  accumulated  an  extensive  litera- 
ture which  we  shall  not  attempt  to  treat  in  detail,  since  it  has 
been  handled  very  fully  by  the  specialists  in  these  subjects. 
We  shall,  however,  present  the  most  important  conclusions  and 

1  This  paper  concludes  the  series  of  studies  on  the  plant  cell.  The  author  has 
a  number  of  complete  sets  of  reprints  of  this  and  the  earlier  sections.  Enquiries 
may  be  addressed  to  Professor  Bradley  M.  Davis,  University  of  Chicago. 

695 


696  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

try  to  give  the  present  status  of  investigations  in  these  most 
difficult  subjects. 

CyanopJiycece  (Blue-green  Algce). —  The  most  recent  and  com- 
prehensive papers  on  the  cell  structure  of  the  Cyanophycese  are 
by  Fischer  ('97),  Macallum  ('99),  Hegler  (:oi),  Biitschli  (:  02), 
Kohl  (:  03),  Zacharias  (:oo,  :  03),  and  Olive  (:O4).  Olive  gives 
an  especially  clear  analysis  of  the  situation  in  this  field  of 
investigation  at  the  present  time  and  an  excellent  historical 
review  of  earlier  literature  may  be  found  in  Regies  (:  01).  The 
discussions  center  chiefly  around  (i)  the  presence  or  absence  of 
a  nuclear  structure  and  its  behavior  in  cell  division,  (2)  the  dis- 
tribution of  the  blue-green  pigment  (phycocyan)  and  the  struc- 
ture of  a  possible  chromatophore,  and  (3)  the  nature  of  certain 
conspicuous  inclusions  within  the  cell,  called  cyanophycin  gran- 
ules and  slime  globules.  An  outline  in  tabular  form  of  the 
views  of  some  thirty  investigators  on  these  subjects  is  given  by 
Olive  (:O4,  p.  10). 

Writers  from  the  earliest  periods  of  cell  studies  on  the  Cyan- 
ophyceae  have  recognized  the  presence  of  a  central  body  in  the 
interior  of  the  cell  more  or  less  sharply  differentiated  from  the 
peripheral  region,  which  holds  the  coloring  matter  and  certain 
inclusions.  The  central  body  contains  granular  material  which 
stains  and  behaves  in  other  particulars  like  chromatin.  But  as 
a  rule  this  granular  material  is  not  confined  within  a  membrane 
or  vacuolar  cavity  which  has  proved  the  most  serious  difficulty 
to  its  acceptance  as  chromatin  and  the  central  body  as  a  nucleus. 
Then  many  investigators  have  not  been  able  to  satisfy  them- 
selves that  the  central  body  exhibits  the  phenomena  character- 
istic of  nuclear  division  even  in  a  simple  form.  Consequently 
much  doubt  has  been  expressed  as  to  its  morphology  and  pos- 
sible relation  to  a  nucleus. 

The  most  recent  and  detailed  investigations  have,  however, 
brought  forward  much  evidence  to  the  effect  that  the  granular 
material  in  the  central  body  is  chromatin  which  becomes  organ- 
ized into  chromosomes  that  are  distributed  by  a  form  of  mitotic 
division.  In  the  vegetative  cells,  which  generally  divide  rapidly, 
the  chromatin  is  never  held  within  a  nuclear  membrane  but  in 
young  heterocysts  and  spores  such  inclosing  membranes  have 
been  found  (Olive,  :  04). 


No.  466.]          STUDIES   ON  PLANT  CELL —  VIII.  697 

Olive  (:  04)  has  given  especial  attention  to  methods  of  sec- 
tioning and  staining  on  the  slide  and  presents  the  most  detailed 
account  of  the  structure  and  behavior  of  the  chromatin-and  the 
simple  apparatus  which  brings  about  the  division  of  the  central 
body.  The  central  body  is  made  up  chiefly  of  dense  kinoplasm 
with  a  fibrillar  structure  in  which  lie  chromosomes  that  may  be 
counted  and  whose  number  is  found  to  be  constant  in  several 
species.  Thus  there  are  eight  chromosomes  in  a  species  of 
Gloeocapsa  and  Nostoc  and  sixteen  in  certain  forms  of  Oscilla- 
toria,  Phormidium,  and  Calothrix.  The  chromatin  in  some 
cases  was  observed  to  be  organized  into  what  seemed  to  be  a 
simple  type  of  spirem  (especially  clear  in  Gloeocapsa)  within  the 
central  body,  and  the  chromosomes  are  formed  by  a  concentra- 
tion of  material  at  certain  points  which  are  constant  in  the  cells 
of  the  same  plant. 

Olive  found  evidence  that  the  chromosomes  split  during  the 
process  of  division  of  the  central  body  and  are  gathered  in  two 
groups  at  the  ends  of  the  achromatic  structure  which  is  gener- 
ally flattened  at  the  poles  and  conforms  in  other  particulars  to 
the  shape  of  the  cells.  The  two  sets  of  chromosomes  are 
finally  separated  by  the  cell  wall  which  develops  from  the  pe- 
riphery during  cell  division  and  cuts  the  achromatic  structure 
in  the  middle  region.  That  portion  of  the  central  body  which 
remains  between  the  two  sets  of  daughter  chromosomes  is 
regarded  by  Olive  as  equivalent  to  the  central  spindle  so  well 
defined  in  stages  of  anaphase  and  telophase  in  mitoses  of  higher 
plants.  The  central  body  during  this  process  of  division  has 
certainly  very  much  the  appearance  of  a  simple  type  of  spindle 
although  there  are  not  present  the  large  fibers  so  characteristic 
of  nuclear  figures  in  higher  plants.  Moreover  it  can  scarcely 
be  held  that  the  division  is  one  of  simple  fusion  when  chromo- 
somes are  present  in  constant  numbers  and  split  into  two  groups 
with  each  division  of  the  cell.  Olive  believes  that  the  achro- 
matic structure,  present  during  cell  division,  is  a  disc-shaped, 
generally  flat-poled  spindle,  densely  fibrous  in  structure  and  that 
the  fission  of  the  chromosomes  and  their  separation  into  two 
sets  constitutes  a  true  mitotic  division  of  the  central  body,  which 
is  a  nucleus. 


698  THE  AMERICAN  NATURALIST.      [VOL.  XXXIX. 

Other  authors  as  Scott  ('88),  Hegler  (:oi),  Butschli  (:  02), 
and  Kohl  (:  03),  also  believe  that  the  central  body  is  a  nucleus 
which  divides  mitotically  but  none  has  described  the  process  as 
so  closely  similar  to  nuclear  division  in  higher  plants  as  in  the 
account  of  Olive.  Some  of  their  results  are  criticized  by  Olive 
as  based  on  preparations  in  which  the  stain  was  not  properly 
differentiated  or  the  sections  were  too  thick.  Among  the  recent 
writers  Wager  (:  03)  stands  alone  as  holding  that  the  nucleus 
divides  directly  (amitotically)  by  a  process  of  simple  fission. 
Both  Kohl  and  Wager  conceive  the  chromatin  as  in  a  network 
or  convolute  spirem  which  breaks  up  into  segments  which  are 
drawn  apart,  thread  by  thread,  quite  a  different  process  from  the 
splitting  of  organized  chromosomes.  Other  authors  have  held 
that  the  granules  in  the  central  body  were  chromatin  although 
they  were  not  willing  to  admit  the  structure  as  a  nucleus.  Thus 
Macallum  ('99)  found  that  the  central  body  contained  phosphor- 
ous and  "masked  iron"  to  a  conspicuous  degree  and  he,  with 
other  investigators,  has  shown  that  this  structure  resists  the 
action  of  artificial  gastric  juice,  solutions  of  pepsin,  etc.  These 
chemical  reactions  are  considered  confirmatory  of  the  theory 
that  the  granular  material  is  a  proteid  of  a  high  order  of  or- 
ganization such  as  would  be  expected  of  chromatin.  However, 
such  chemical  tests  are  very  difficult  to  apply  and  do  not  seem  to 
the  writer  so  important  in  establishing  the  nature  of  the  central 
body  as  does  the  careful  study  of  its  structure  and  activity  during 
cell  division.  The  objection  that  the  central  body  lacks  a  mem- 
brane, universally  present  around  resting  nuclei  of  higher  plants, 
is  not  regarded  as  vital  by  Olive.  In  the  first  place  such  a 
membrane  may  be  found  around  the  resting  nuclei  in  young 
heterocysts  and  spores  and  its  absence  in  vegetative  cells  is 
probably  explained  by  the  rapidity  of  the  successive  cell  divi- 
sions. There  are  some  recent  writers,  as  Massart  (:  02)  and 
Zacharias  (:  oo,  :  03)  who  are  still  unconvinced  that  the  granules 
in  the  central  body  are  chromatin  and  that  the  structure  is  the 
equivalent  of  a  nucleus.  Their  papers  and  figures,  however, 
clearly  show  that  they  have  failed  to  find  the  detailed  structures 
of  other  investigators. 

Fischer  ('97)  has  been  the  most  conspicuous  opponent  of  the 


No.  466.]  STUDIES   ON  PLANT  CELL.—  VIII.  699 

view  that  the  cells  of  the  Cyanophyceae  and  also  of  the  Schizo- 
mycetes  contain  nuclei,  taking  a  position  in  sharp  opposition  to 
that  of  BUtschli  ('96).  Fischer's  conclusions  were  based  on  his 
failure  to  find  that  differentiation  of  the  protoplasm  within  the 
cell  demanded  by  the  conception  of  the  central  body  and  the 
activities  of  this  structure  during  cell  division  as  described  by 
other  authors.  He  presented  a  sharp  criticism  of  the  conclu- 
sions based  on  the  reaction  of  stains  in  determining  the  nature 
of  protoplasmic  structures,  criticisms  largely  directed  against  the 
investigations  of  Biitschli.  He  showed  by  some  ingenious  experi- 
ments upon  emulsions  of  albumen  fixed  on  a  slide  that  stain 
reactions  were  a  purely  physical  phenomenon.  Thus  the  same 
combinations  of  stains,  such  as  saffranin  and  gentian  violet,  may 
be  made  to  give  exactly  opposite  results  in  differentiating  a  mix- 
ture of  large  and  small  globules  of  albumen  when  used  in  reverse 
order.  He  attached  no  importance  to  the  so  called  affinity  of  a 
protoplasmic  structure  for  a  particular  stain  and  would  not  accept 
such  apparent  affinity  as  evidence  of  its  chemical  nature.  The 
fact  that  the  central  body  takes  chromatic  stains  did  not  seem  to 
him  important  evidence  of  its  nuclear  character  and  he  was  very 
positive  in  his  belief  that  the  cells  of  the  Cyanophyceae  do  not 
contain  nuclei  and  that  the  central  bodies  should  not  be  consid- 
ered the  phylogenetic  forerunners  of  such  structures. 

This  attitude  of  Fischer  towards  conclusions  based  on  stain 
reactions  was  later  presented  in  more  elaborate  form  in  his  cri- 
tique ('99)  on  methods  of  fixing  and  staining  protoplasm  and  has 
had  an  important  influence  on  methods  of  cytological  investi- 
gation and  interpretation.  The  stain  reaction  is  now  regarded 
as  probably  merely  a  physical  phenomenon  but  an  effective 
means  of  differentiating  protoplasmic  structures.  The  deter- 
mination of  their  morphology  rests  with  an  understanding  of 
their  history  and  behavior  in  the  activities  of  the  cell.  Although 
Fischer's  general  criticism  of  methods  of  cell  research  was 
timely  and  in  some  instances  richly  deserved,  nevertheless  his 
particular  conclusions  respecting  the  cell  structure  of  the  Cyano- 
phyceae and  the  Schizomycetes  have  not  been  sustained  by 
investigators  who  have  followed  the  history  of  the  protoplasmic 
structures  in  the  cells  of  these  organisms. 


700  THE  AMERICAN  NATURALIST.      [VOL.  XXXIX. 

We  may  pass  now  to  the  peripheral  region  of  the  cell  which 
holds  the  blue-green  coloring  matter  of  the  Cyanophyceae.  A 
number  of  investigators,  as  Wager  (103),  Kohl  (103),  Hegler 
(:oi),  and  Hieronymus  ('92),  have  held  that  this  pigment  was 
contained  in  minute  granules  distributed  throughout  the  cyto- 
plasm under  the  cell  wall.  These  granules  have  at  times  been 
termed  chromatophores  or  plastids  and  Hegler  has  proposed  for 
them  the  name  cyanoplastids.  Other  authors,  especially  Fischer 
('97),  Nadson  ('95),  Palla  ('93),  and  Zukal  ('92)  have  been  unable 
to  find  these  color-bearing  granules  and  have  believed  the  color- 
ing matter  to  be  uniformly  diffused  throughout  the  peripheral 
region  of  the  cell.  Fischer  has  made  a  particularly  thorough 
study  of  the  reactions  of  the  pigmented  region  to  various  acids 
in  comparison  with  the  chromatophores  of  higher  algae  and  con- 
cludes that  no  plastids  are  present  but  that  the  color  is  held  in  a 
hollow  cylindrical  or  spherical  outer  layer  of  protoplasm  which 
may  be  termed  a  chromatophore.  Olive  supports  Fischer, 
approaching  the  subject  from  a  very  different  point  of  view.  If 
minute  plastids  are  present  they  should  be  visible  in  fixed  and 
stained  material  and  Olive  is  unable  to  find  any  trace  of  Hegler's 
cyanoplasts.  The  granules  .of  the  outer  region  of  the  protoplast 
seem  to  be  colorless  inclusions. 

Perhaps  the  most  confused  part  of  the  discussion  on  the 
structure  of  the  cell  of  the  blue-green  algae  is  that  which  deals 
with  certain  inclusions.  There  are  apparently  two  sorts  which 
are  very  common  in  the  cells:  (i)  the  cyanophycin  granules 
(Borzi)  and  (2)  the  slime  globules.  The  cyanophycin  granules 
are  very  apt  to  lie  along  the  cross  walls  in  filamentous  forms  or 
in  other  peripheral  regions  of  the  cell.  They  are  generally 
believed  to  be  a  form  of  food  material  and  it  has  been  suggested 
that  they  are  the  first  visible  product  of  photosynthetic  processes, 
but  their  chemical  nature  is  under  dispute.  The  slime  globules 
lie  more  frequently  in  the  interior  region  of  the  cell  close  to  the 
nucleus  and  frequently  within  this  structure.  They  have  been 
termed  nucleoli  by  some  authors  and  also  confused  with  chro- 
matin.  Besides  these  two  bodies,  other  minute  globules  have 
been  described  as  oil  or  fat  and  some  remarkable  crystalloid 
structures  have  been  figured,  especially  by  Hieronymus  ('92)- 


No.  466.]          STUDIES   ON  PLANT  CELL.— VIII.  701 

Indeed  the  entire  subject  is  so  confused  that  it  does  not  seem 
desirable  for  us  to  take  it  up  in  detail  at  this  time,  especially 
since  these  inclusions  are  apparently  all  secretions  or  excretions 
and  not  morphological  features  of  the  cell.  The  most  compre- 
hensive discussions  of  the  subject  will  be  found  in  the  papers  of 
Hegler  (:oi),  Kohl  (:O3),  and  Zacharias  (:  03). l 

Schisomycetcs  {Bacteria). — The  history  of  research  upon  the 
cell  structure  of  the  Schizomycetes  has  run  in  large  part  parallel 
with  that  on  the  Cyanophycese.  The  clearest  results  have  come 
from  studies  upon  the  larger  forms  of  the  sulphur  bacteria, 
especially  certain  species  of  Beggiatoa,  and  on  certain  forms  of 
Spirillum.  The  more  minute  types  and  pathogenic  forms' in  par- 
ticular have  proved  very  baffling  because  of  their  small  size  and 
it  can  scarcely  be  said  that  we  fully  understand  their  cell  struc- 
ture. As  in  the  Cyanophyceae,  investigators  of  the  bacteria  fall 
into  two  groups  :  one  holding  that  the  Schizomycetes  entirely 
lack  a  nucleus  and  the  other  that  there  is  present  a  structure, 
often  termed  a  central  body,  which  is  the  equivalent  of  a  nucleus. 

Biitschli  ('96,  :  02)  has  been  the  most  conspicuous  advocate 
of  the  latter  view.  He  described  and  figured  clearly  a  central 
body  in  the  cells  of  Beggiatoa,  Chromatium,  and  Spirillum  with 
the  same  organization  as  given  in  his  account  of  that  body  in  the 
Cyanophyceae.  The  central  body  contains  granular  material 
which  Biitschli  regards  as  chromatin  and  the  structure  is  shown 
in  stages  of  division.  Biitschli  has  no  hesitation  in  giving  the 
central  body  the  value  of  a  nucleus.  It  lies  within  a  peripheral 

1  Since  the  above  was  written  a  lengthy  paper  by  Fischer,  "  Die  Zelle  der 
Cyanophyceen  "  has  appeared  (Bot.  Zeit.,  vol.  63,  p.  51,  1905),  too  late  to  be 
included  in  these  reviews.  Fischer  has  not  changed  his  conclusions  on  the  chief 
points  as  discussed  in  his  earlier  papers.  The  chromatophore  is  a  closed  cylin- 
drical structure  ;  the  cyanophycin  granules  are  proteid  in  character  ;  glycogen  and 
another  carbohydrate,  anabasnin,  aie  conspicuous  substances  in  the  cell;  the 
central  body  is  not  a  nucleus  but  the  seat  of  important  metabolic  processes  con- 
cerned with  these  carbohydrates,  and  its  contents  and  behavior  in  cell  division 
have  only  a  superficial  resemblance  to  nuclear  structure  and  mitosis ;  the  chro- 
matin granules  of  Hutschli,  Olive,  and  others  are  masses  of  anabsenin  (a  car- 
bohydrate). Fischer's  criticisms  are  fundamental  and  it  is  evident  that  the 
morphologists  must  clearly  establish  the  proteid  nature  of  the  central  body  and 
its  contents  (especially  the"  so  called"  chromatin  granules)  before  they  can 
expect  the  acceptance  of  their  conclusions  as  to  its  nuclear  character. 


702  THE   AMERICAN  NATURALIS7\        [VOL.  XXXIX. 

region  of  protoplasm  as  in  the  Cyanophyceae.  There  is  of  course 
no  blue-green  pigment  (phycocyan)  in  the  cells  of  bacteria  and 
consequently  no  chromatophore  but  several  sorts  of  inclusions 
may  be  present  in  the  protoplasm.  The  nature  of  some  of  the 
inclusions  is  not  clear  and  this  subject  has  not  been  given  as 
much  attention  as  in  the  Cyanophyceae.  It  is  significant  that 
this  cell  structure  should  be  found  so  clearly  in  the  Beggiatoa 
since  this  organism  seems  very  close  to  Oscillatoria  in  its  mor- 
phology. Some  of  the  larger  species  of  Beggiatoa  may  be 
expected  to  yield  conclusions  similar  to  those  of  Olive's  investi- 
gation on  Oscillatoria  if  sectioned  and  critically  stained,  especi- 
ally as1  the  cells  are  very  large  in  some  forms  and  there  is 
probably  less  extraneous  matter  to  complicate  the  interpretation 
of  the  preparations. 

As  has  been  stated,  investigations  upon  the  smaller  species  of 
bacteria  and  especially  upon  pathogenic  forms  have  met  with 
great  difficulties.  These  led  at  one  time  to  the  ingenious  theory 
of  Biitschli  ('90),  followed  by  Zettnow  ('97)  that  possibly  the 
entire  protoplast  had  the  value  of  a  nucleus.  That  is  to  say, 
an  outer  peripheral  region  of  cytoplasm  had  either  never  been 
developed  in  these  organisms  or,  if  present,  had  become  so 
closely  associated  with  the  chromatin  that  it  could  not  be  dis- 
tinguished as  a  special  region  of  the  cell.  A  peripheral  region 
of  cytoplasm  is  represented  in  some  of  the  larger  forms  by  the 
cilia  and  by  accumulations  of  protoplasm  at  the  ends  of  the  cells, 
especially  clearly  shown  in  Spirillum  (Biitschli,  '96  ;  Zettnow, 
'97).  Later  Zettnow  ('99)  and  Feinberg  (:  oo)  applying  the 
staining  method  of  Romanowski,  followed  by  several  later  inves- 
tigators with  improved  technique  (Nakanishi,  :oi,and  others), 
succeeded  in  differentiating  a  minute  body  in  the  cells  of  smaller 
bacteria  and  pathogenic  forms,  which  is  regarded  now  as  similar 
to  the  central  body  of  the  sulphur  bacteria  and  a  true  nucleus. 
This  structure  is  very  minute  since  it  occupies  a  portion  of 
these  exceedingly  small  cells.  Naturally  it  will  be  very  difficult 
to  obtain  any  detailed  knowledge  of  its  structure  and  behavior 
during  cell  division.  But  enough  seems  to  be  known  to  justify 
the  belief  that  differentiated  nuclear  structures  are  probably 
present  even  in  the  smallest  types  of  bacteria.  A  recent  paper 


No.  466.]          STUDIES   ON  PLANT  CELL.—  VIII.  703 

of  Vejdovsky  (:  04)  describes  and  figures  a  simple  type  of  spindle 
in  Bacterium  gammeri  and  Bryodrilus  eJilersi  with  a  separation 
of  two  groups  of  chromatin  granules  during  mitosis~ 

The  chief  critics  of  the  conclusions  that  the  cells  of  Schizo- 
mycetes  are  nucleated  have  been  Migula  ('95)  and  Fischer. 
The  latter  author  in  particular  has  devoted  considerable  attention 
to  the  group  especially  in  his  paper  of  1897  which  is  largely  a 
discussion  of  Biitschli's  ('96)  results  on  studies  of  the  blue-green 
algae  and  bacteria.  Fischer  considers  the  central  body  described 
by  Biitschli  in  the  sulphur  bacteria  as  merely  a  vacuolate  region 
of  the  cell  made  conspicuous  by  the  arrangement  of  the  sulphur 
grains  and  that  the  structure  does  not  appear  in  cells  which  are 
free  from  sulphur.  The  granular  material,  considered  as  chro- 
matin by  others,  is  regarded  by  Fischer  as  reserve  material. 
The  central  body  described  by  Biitschli  in  the  cells  of  Spirillum 
is  stated  to  be  a  product  of  contraction.  In  general  the  same 
criticism  which  Fischer  applied  to  the  methods  of  staining  and 
interpretation  of  structures  in  the  Cyanophyceae  is  presented  for 
the  Schizomycetes.  Fischer  cannot  justify  Biitschli's  ('90)  view 
that  the  smaller  bacteria  are  chiefly  composed  of  nuclear  sub- 
stance, a  view  which  probably  has  few  if  any  followers  to-day 
and  could  scarcely  claim  to  be  more  than  a  passing  suggestion. 
In  short,  Fischer  finds  no  evidence  of  a  nuclear  structure  in  the 
Schizomycetes  but  curiously  ends  by  declaring  that  the  group 
has  no  affinities  with  the  Cyanophyceae  but  that  its  forms  are 
closely  associated  with  the  Flagellata. 

SaccJiaromycetes  (Yeasts]. —  The  structure  of  the  yeast  cell 
has  been  perhaps  the  subject  of  as  long  a  series  of  investigations 
as  the  cells  of  the  Cyanophyceae  and  Schizomycetes,  and  the 
problems  in  both  cases  have  many  similar  features.  The  chief 
problem  in  the  yeasts  has  concerned  the  presence  or  absence  of 
an  organized  nucleus  or  its  equivalent  in  the  form  of  some  sim- 
pler structure.  The  accounts  range  from  a  complete  denial  of 
its  presence  to  descriptions  of  a  nuclear  apparatus  of  considera- 
ble complexity  which  passes  through  some  rather  involved  activi- 
ties during  cell  division.  It  is  impossible  for  us  to  treat  the 
subject  historically.  We  shall  only  consider  the  accounts  of  the 
most  recent  investigators  and  try  to  determine  the  probable 


704  THE   AMERICAN  NATURALIST.       [VoL.  XXXIX. 

bearing  of  these  studies.     An  admirable  review  of  the  early  lit- 
erature is  presented  in  Wager's  paper  of  1898. 

Wager  ('98)  himself  has  made  one  of  the  most  detailed  studies 
of  the  yeast  cell  and  his  conclusions  on  the  presence  of  a 
"  nuclear  apparatus  "  will  be  made  the  starting  point  of  our  dis- 
cussion. The  yeast  cell  contains  a  structure,  termed  by  Wager 
a  "  nuclear  body,"  generally  situated  at  one  side,  close  to  the 
cell  wall.  This  body  resembles  the  nucleolus  of  higher  plants  in 
its  homogeneous  structure  and  reaction  to  stains.  Besides  the 
"  nuclear  body "  Wager  finds  a  vacuole  always  present  which 
contains  granular  material  and  is  an  important  part  of  the  nuclear 
apparatus.  This  "  nuclear  vacuole-"  must  be  carefully  distin- 
guished from  other  vacuoles  of  the  usual  type  which  merely  con- 
tain glycogen.  There  are  besides  some  globular  bodies  in  the 
protoplasm  whose  nature  may  be  oil  in  some  cases  and  proteid  in 
others.  The  "nuclear  body"  is  always  in  close  contact  with  the 
"  nuclear  vacuole  "  but  is  never  within  it.  The  amount  of  granu- 
lar material  in  the  nuclear  vacuole  is  variable  but  it  sometimes 
contains  a  dense  mass.  This  content  is  believed  to  be  chroma- 
tin  from  the  behavior  to  stains  and  insolubility  in  digestive 
fluids.  Sometimes  the  nuclear  vacuole  disappears  but  in  such 
cases  the  granular  network  is  found  in  contact  with  the  nuclear 
body  and  sometimes  distributed  about  it  in  a  very  regular  man- 
ner. The  chromatic  granular  material  appears  then  to  be  a  per- 
manent substance  in  the  cell  and  always  closely  associated  with 
the  nuclear  body,  sometimes  distributed  about  it  and  sometimes 
included  within  a  special  vacuole. 

Wager  concludes  that  the  nuclear  apparatus  consists  of  (i)  a 
nucleolus  (nuclear  body)  and  (2)  a  store  of  chromatin  in  a  net- 
work, either  enclosed  in  a  vacuole  in  close  contact  with  the 
nucleolus  or  lying  freely  about  the  nucleolus  or  sometimes 
disseminated  in  granules  generally  throughout  the  cytoplasm. 
Wager  believes  that  the  nuclear  vacuole  arises  from  the  fusion 
of  numerous  small  vacuoles  which  lie  around  the  chromatin  gran- 
ules which  thus  come  to  lie  within  a  common  vesicle.  This 
mode  of  origin  seems  reasonable  from  what  we  know  of  the 
history  of  the  nuclear  vacuole  which  arises  around  the  chromo- 
somes that  gather  at  anaphase  of  mitosis  to  form  daughter 


No.  466.]          STUDIES  ON  PLANT  CELL.—  VIII.  705 

nuclei  in  higher  plants.  The  earlier  investigators  for  the  most 
part  failed  to  recognize  the  chromatic  granules  and  network 
and  considered  the  nucleolar  body  (nucleolus)  to  be  ^the-  nucleus 
of  the  cell.  Janssens  and  Leblanc  ('98),  however,  described  a 
nucleus  with  a  membrane  containing  caryoplasm  and  a  nucleolus, 
and  other  authors  noted  the  vacuole  and  believed  that  it  held 
some  relation  to  the  nucleus. 

Both  the  nuclear  vacuole  and  the  nuclear  body  (nucleolus) 
take  part  in  the  process  of  bud  formation.  The  bud  appears  on 
the  opposite  side  of  the  cell  from  the  nuclear  body  and  the  nu- 
clear vacuole  lies  between.  The  bud  contains  at  first  cytoplasm 
alone ;  then  the  nuclear  vacuole  begins  to  pass  into  it  and  the 
nuclear  body  takes  a  position  in  the  vicinity,  between  the 
mother-cell  and  the  bud.  The  nuclear  body  now  divides  by 
simple  fission  and  one  half  enters  the  bud.  The  nuclear  vacu- 
ole gradually  constricts  and  is  drawn  apart  in  the  canal  between 
the  two  cells.  The  two  daughter  nuclear  vacuoles  and  nuclear 
bodies  then  pass  to  opposite  ends  of  the  mother-  and  daughter- 
cells  respectively.  If  the  nuclear  vacuole  is  absent  the  chroma- 
tin  network  is  drawn  apart  so  that  a  division  is  effected  in  a 
similar  manner. 

At  the  time  of  spore  formation,  the  chromatin  is  reported  by 
Wager  to  become  so  closely  associated  with  the  nuclear  body 
that  the  two  substances  cannot  be  easily  separated  and  behave 
as  one.  The  resultant  structure  elongates  and  divides  by  con- 
striction and  the  subsequent  divisions  are  of  the  same  character. 
Strands  of  deeply  staining  protoplasm  between  the  daughter 
nuclei  are  of  interest  as  suggesting  the  possibility  of  a  simple 
type  of  spindle.  Wager  describes  the  formation  of  spore  walls 
around  the  nuclei  enclosing  a  portion  of  the  protoplasm  and 
thus  cutting  the  spores  out  from  the  remaining  non-nucleate  cell 
contents.  The  details  of  this  process  are  not  known  and  might 
prove  very  interesting  since  the  process,  from  W'ager's  account, 
would  seem  to  be  one  of  free  cell  formation  without,  however, 
the  characteristics  described  by  Harper  in  spore  formation 
within  the  ascus.  It  should  be  more  thoroughly  studied  for  it 
is  possible  that  the  division  will  be  found  to  involve  cleavage 
furrows  and  really  prove  to  be  a  type  of  segmentation  by  con- 
striction (Section  II,  Amer.  Nat.,  vol.  38,  p.  453,  June,  1904). 


706  THE   AMERICAN  NATURALIST.        [VoL.  XXXIX. 

Several  papers  have  appeared  on  the  structure  of  the  yeast 
cell  since  Wager's  account  of  1898.  Marpmann  (:O2)  and 
Feinberg  (:  02)  described  much  simpler  conditions  than  are 
reported  by  Wager,  and  recognize  scarcely  more  than  a  deeply 
staining  body  which  they  term  a  nucleus.  Hirschbruch  (:  02) 
gives  an  extraordinary  description,  accompanied  by  diagram- 
matic figures,  of  a  nuclear  structure  and  a  body,  staining  red 
and  blue  respectively,  which  are  supposed  to  fuse  previous  to 
the  development  of  a  bud,  but  the  account  is  so  unsatisfactory 
as  to  merit  little  attention.  Janssens  (:O3)  reviews  the  work  of 
these  investigators  and  others  in  comparison  with  his  earlier 
results  (Janssens  and  Leblanc,  '98).  Guilliermond  (:O4)  has 
published  the  most  recent  paper  presenting  more  completely  his 
conclusions  of  an  earlier  investigation  in  1902. 

Guilliermond's  conclusions  have  some  points  of  resemblance 
to  those  of  Wager.  He  finds  a  nuclear  vacuole  containing  a 
granular  network  believed  to  be  chromatin  and  a  nucleolar 
structure.  The  entire  body  seems  to  be  a  true  nucleus,  not  dif- 
fering in  its  essentials  from  the  nuclei  of  other  fungi.  Some- 
times all  the  material  in  the  nucleus  seems  to  be  condensed  into 
a  central  body,  a  sort  of  chromatin  nucleolus  (chromoblast) 
somewhat  resembling  a  similar  structure  in  Spirogyra.  Guillier- 
mond figures  the  nucleus  as  constricting  during  the  process  of 
•  budding,  one  part  passing  into  the  daughter  cell.  His  figures 
show  clearly  deeply  stained  material  outside  of  the  nuclear 
membrane  in  a  position  similar  to  that  of  Wager's  nucleolar 
body  (nucleolus). 

These  points  of  agreement  seem  to  justify  at  least  in  part 
Wager's  account,  but  of  course  the  peculiarities  of  both  lead 
one  to  suspect  that  there  are  important  features  in  the  structure 
of  the  nucleus  and  in  the  events  of  nuclear  division  which  have 
not  been  determined.  It  certainly  seems  probable  that  chroma- 
tin  is  present  in  definitely  organized  bodies  (chromosomes)  some- 
times within  a  vacuole  and  sometimes  lying  around  a  nucleolar 
structure.  The  latter  also  holds  an  intimate  relation  to  the 
chromatin,  which  is  frequently  true  in  higher  plants.  There  are 
indications  that  a  simple  type  of  spindle  is  present  at  least  in 
the  nuclear  divisions  during  spore  formation.  In  view  of 


No.  466.]  STUDIES   ON  PLANT  CELL.—  VIII.  707 

Olive's  results  in  studies  on  the  Cyanophycese  it  does  not 
seem  unreasonable  to  hope  that  more  accurate  staining  of  very 
thin  sections  will  bring  the  peculiarities  of  these  accounts  into 
harmony  with  mitotic  phenomena  of  higher  forms. 

The  accounts  of  conjugation  in  yeasts  (Barker,  :oi  and 
.Guilliermond,  103)  which  were  discussed  under  "Asexual  Cell 
Unions  and  Nuclear  Fusions  "  in  Section  IV  give  no  additional 
information  on  the  essential  structure  of  the  yeast  cell. 

2.    COMPARISONS  OF  THE  STRUCTURE  OF  SOME  HIGHER  TYPES 
OF  PLANT  CELL  WITH  SIMPLER   CONDITIONS. 

Some  of  the  most  fruitful  and  interesting  fields  of  investiga- 
tion in  cell  structure  are  likely  to  be  in  those  border  groups 
between  the  very  simplest  conditions  of  the  lower  algae  and 
fungi  and  the  higher  regions  where  the  nucleus  and  processes  of 
mitosis  have  clearly  the  essential  features  which  are  generally 
ascribed  to  this  structure  and  its  activities.  At  present  the  gap 
seems  very  great  between  the  simple  conditions  of  the  Schizo- 
phyta  and  the  groups  of  algae  and  fungi  on  the  next  higher 
general  level.  But  as  a  matter  of  fact  we  know  almost  noth- 
ing of  the  nuclear  structure  in  the  lowest  groups  of  the  Chloro- 
phyceae,  i.  e.,  among  the  simplest  of  the  unicellular  green  algae. 
It  is  rather  remarkable  that  this  region  should  have  been 
so  neglected. 

The  Nucleus. —  Comparative  studies  on  the  nucleus  naturally 
treat  chiefly  of  the  chromosomes  and  nucleolus.  One  of  the 
most  interesting  features  of  more  recent  research  on  the  nucleus 
has  been  the  steady  accumulation  of  evidence  indicating  that  the 
nucleolus  holds  a  very  important  relation  to  the  chromatin  con- 
tent. There  are  types  among  the  lower  algae  in  which  the  whole 
or  a  greater  part  of  the  chromatin  is  gathered  into  a  dense  nu- 
cleolar  body  in  the  resting  nucleus.  Spirogyra  is  the  best- 
known  illustration  of  this  condition  and  has  been  studied  by 
several  investigators.  Similar  phenomena  have  been  reported 
by  myself  in  Corallina  (Davis,  '98),  by  Golenkin  ('99)  for 
Sphaeroplea,  and  by  Wolfe  (:  04)  for  Nemalion.  Some  nuclei, 
however,  particularly  in  the  higher  plants  have  nucleoli  whose 


708  THE  AMERICAN  NATURALIST.      [VOL.  XXXIX. 

substance  does  not  seem  to  contribute  directly  to  the  chromo- 
somes and  these  have  been  regarded  as  secretions  within  the 
nucleus.  Strasburger  believed  that  such  were  masses  of  reserve 
material  drawn  upon  by  the  kinoplasm  during  the  process  of 
spindle  formation.  The  term  plastin  has  been  applied  to  such 
substance  in  the  nucleolus  and  also  in  the  linin  as  cannot  be 
directly  connected  with  chromatin.  A  nucleolus  may  consist  of 
plastin  alone,  or  have  with  this  substance  varying  quantities  of 
chromatin.  Nucleoli  consisting  of  chromatin  alone  may  be  ex- 
pected among  the  lower  plants  from  the  studies  on  Spirogyra, 
Corallina,  Sphaeroplea,  and  Nemalion.  Plastin  and  chromatin 
are  probably  closely  related  substances. 

A  recent  paper  of  Wager  (:  04)  indicates  that  the  nucleolus 
of  some  higher  plants  holds  a  far  closer  relation  to  the  chromo- 
somes than  has  been  supposed  and  rather  weakens  Strasburger' s 
theory  of  the  structure  as  a  reserve  mass  drawn  upon  during 
mitotic  activities.  This  study  and  recent  papers  by  Miss  Mer- 
riman  (:  04)  and  Mano  (:  04)  have  all  been  upon  the  cells  of  root 
tips  while  the  conceptions  of  Strasburger  and  others  have  been 
founded  largely  on  the  structure  and  behavior  of  the  nucleolus 
in  the  spore  mother-cell  during  the  mitoses  of  sporogenesis. 
Wager  treats  of  the  root  tip  of  Phaseolus,  Miss  Merriman  of 
Allium,  and  Mano  of  Solanum  and  Phaseolus.  They  are  impor- 
tant contributions  to  the  subject  of  the  nucleolus  and  should  be 
considered  in  any  treatment  of  this  structure.  The  papers 
appeared  too  recently  to  be  noted  in  our  brief  account  of 
the  nucleolus  in  Section  I  which  is  consequently  incomplete. 
Wager's  paper  especially  presents  an  excellent  review  of  the 
literature  on  the  nucleolus  in  the  plant  cell. 

Wager  concludes  that  the  nucleolus  is  really  a  portion  of  the 
nuclear  network  and  that  the  spirem  is  derived  in  part  at  least 
from  this  structure.  Material  from  the  nucleolus  then  passes 
into  the  chromosomes.  Also,  in  the  reconstruction  of  the 
daughter  nuclei  the  chromosomes  are  massed  together  at  a  cer- 
tain stage  and  from  this  mass  the  nucleolus  emerges,  taking  out 
with  it  the  greater  part  of  the  chromatin.  Wager  then  con- 
siders the  nucleolus  as  a  store  of  chromatin  which  must  be 
taken  into  account  in  theories  of  heredity  based  on  the  morpho- 


No.  466.]          STUDIES   ON  PLANT  CELL.—  VIII.  709 

logical  independence  of  the  chromosomes.  Miss  Merriman 
reports  the  origin  of  the  nucleoli  as  masses  among  the  meshes 
of  chromatin  from  which  they  draw  their  substance.  TMafio,  in 
contrast  to  Wager,  holds  that  the  nucleoli  appear  as  globules 
independent  ot  the  chromatin  network  and  later  flow  together 
into  a  single  body.  The  chromosomes  are  also  believed  by 
Mano  to  be  morphologically  independent  of  the  nucleolus  and 
if  the  latter  furnishes  material  to  the  former  it  is  not  by  the 
emergence  of  strands  as  described  by  Wager.  Mano  then  holds 
the  nucleolus  to  be  an  accessory  structure  without  morphologi- 
cal relation  to  the  chromosomes. 

The  theory  of  the  individuality  of  the  chromosomes  is  of 
course  vitally  concerned  with  the  problem  of  the  morphology  of 
the  nucleolus  but  this  topic  we  have  reserved  for  later  treatment 
under  the  caption  :  "  The  Essential  Structures  of  the  Plant  Cell 
and  their  Behavior  in  Ontogeny."  The  chromatin  and  nucleoli 
within  the  nucleus  of  a  higher  plant  lie  in  a  vacuole  whose  fluid 
content  is  bounded  by  a  plasma  membrane  similar  to  that  around 
any  vacuole  in  the  cell.  Lawson  (:  03)  and  Gregoire  and 
Wygaerts  (:O3)  have  emphasized  this  structural  condition  in 
recent  papers  but  the  central  idea  seems  to  be  an  old  one  run- 
ning through  the  writings  of  Strasburger  from  an  early  period. 

We  bring  up  these  striking  conceptions  of  nuclear  structure 
in  the  higher  plants  because  it  seems  very  probable  that  a  much 
clearer  understanding  of  the  problems  will  come  through  inves- 
tigations upon  the  simpler  conditions  in  the  lower  plants. 
There,  we  may  hope  to  find  evidence  of  the  primitive  forms  of 
nucleolar  and  chromatic  associations  with  perhaps  some  clues  as 
to  the  manner  of  the  development  of  the  higher  types  of  struc- 
ture. Thus  the  yeast  cell,  as  reported  by  Wager  ('98)  with  its 
chromatin  sometimes  collected  within  a  vacuole  and  sometimes 
distributed  in  the  cytoplasm  and  a  nuclear  body  (nucleolus)  in 
close  association  with  the  nuclear  vacuole,  but  not  within,  is  of 
the  greatest  interest  as  presenting  intermediate  stages  in  the 
complexity  of  nuclear  structure  and  illustrates  what  may  be 
hoped  from  further  research  among  the  lower  forms. 

The  Chromatophore  and  Plastid. —  In  considering  the  great 
variety  of  chromatophores  and  plastids  exhibited  among  the 


710  THE  AMERICAN  NATURALIST.        [VOL.  XXXIX. 

thallophytes  one  notices  at  once  certain  features  of  their  distri- 
bution in  various  groups.  The  large  chromatophores  are  charac- 
teristic of  the  cells  of  simpler  and  more  primitive  groups  and  the 
small  plastids,  numerous  in  the  cells,  are  generally  present  in 
types  which  are  at  a  fairly  high  evolutionary  level.  There  are 
exceptions  of  course  to  this  general  statement  but  some  of 
these  are  probably  significant  of  phylogenetic  relations. 

The  evidence  all  indicates  that  the  "primitive  type  of  chroma- 
tophore  was  a  large  structure  in  the  peripheral  region  of  the 
protoplast  and  with  an  ill  denned  boundary  or  occupying  the 
entire  surface  of  the  cell.  This  type  of  structure  is  at  present 
characteristic  of  chromatophores  of  the  Cyanophycese  and  is  also 
present  in  numbers  of  the  lower  groups  of  green  algae.  Thus 
we  may  find  many  types  in  the  Pleurococcaceae  whose  cells  con- 
tain a  pigment  so  diffused  that  it  is  impossible  to  establish 
definite  limits  and  similar  conditions  often  appear  in  the  cells  of 
some  of  the  higher  algae  as  in  Hydrodictyon  and  certain  simple 
forms  of  the  Ulothncacese. 

The  simple  diffused  types  of  chromatophores  of  the  lower 
algae  become  replaced  in  higher  groups  either  by  sharply  differ- 
entiated structures  of  definite  form  and  often  showing  internal 
organization  in  the  form  of  pyrenoids  or  by  numerous  plastids. 
There  is  considerable  evidence  that  the  plastids  have  arisen  by 
the  successive  splitting  or  division  of  large  organized  chromato- 
phores. The  most  highly  differentiated  chromatophores  are 
found  in  the  Conjugales  and  the  remarkable  size  and  symmetry 
of  these  cells  is  emphasized  by  the  same  peculiarities  of  the 
chromatophores.  They  are  generally  so  placed  in  the  cells  as  to 
give  an  almost  perfect  balance  of  protoplasmic  structure.  This 
principle  is  especially  clearly  illustrated  among  the  desmids  and 
in  such  forms  as  Zygnema  and  Mougeotia  while  even  Spirogyra 
illustrates  the  principle  strikingly  in  the  distribution  of  its  spi- 
rally wound  chromatophores. 

Plastids  are  characteristic  of  the  Siphonales,  Charales,  most 
of  the  Rhodophyceae,  the  higher  Phaeophyceae,  and  all  groups 
generally  above  the  thallophytes.  It  seems  to  be  the  type  of 
structure  best  suited  to  cell  activities  since  with  few  exceptions 
it  is  found  in  groups  in  the  highest  lines  of  plant  evolution  in 


No.  466.]          STUDIES   ON  PLANT  CELL.—  VIII.  7 1  I 

various  directions.  The  only  striking  exceptions  to  this  broad 
principle  are  Anthoceros,  whose  cells  contain  each  a  single  large 
chromatophore,  and  Selaginella.  Selaginella  is  especially  inter- 
esting for,  while  the  cells  of  the  meristematic  region  and  young 
organs  contain  but  a  single  chromatophore,  this  structure  may 
divide  later  in  some  types  to  form  a  chain  of  discoid  plastids  in 
older  cells  connected  with  one  another  by  delicate  strands  of 
protoplasm.  Thus  in  the  life  history  of  certain  species  of  Sela- 
ginella we  have  plainly  shown  the  change  from  a  single  chroma- 
tophore to  a  number  of  plastids.  It  seems  probable  that  this 
history  repeats  in  general  outline  the  evolutionary  history  of  the 
condition  characterized  by  numerous  plastids  within  a  cell  from 
a  primitive  type  of  cell  structure  with  but  a  single  chromato- 
phore. Anthoceros  and  Selaginella  may  be  regarded  as  forms 
whose  cells  still  retain  the  primitive  conditions  with  respect  to 
the  single  large  chromatophore.  There  are  somewhat  similar 
illustrations  in  the  Rhodophyceae  as  in  Nemalion  and  Batracho- 
spermum  whose  cells  hold  a  single  large  chromatophore  while 
most  of  the  more  highly  organized  red  algae  have  numerous 
plastids.  A  beautiful  series  of  stages  illustrating  the  evolu- 
tionary principles  outlined  above  might  be  worked  out  in  the 
Phaeophyceas. 

What  is  the  fundamental  principle  underlying  the  substitution 
of  numerous  plastids  in  a  cell  in  place  of  a  single  chromato- 
phore ?  The  author  believes  that  it  must  have  relation  to  the 
preservation  within  large  cells  of  a  certain  balance  of  the  meta- 
bolic centers.  The  fission  of  a  plastid  is  a  process  of  constric- 
tion and  studies  on  Anthoceros  (Davis,  '99,  p.  94)  indicate 
that  the  bounding  cytoplasmic  membrane  exerts  pressure  upon 
the  elongating  structure.  It  seems  probable  that  the  division  is 
due  to  the  mechanical  separation  of  material  that  is  too  bulky 
for  the  most  effective  results  of  photosynthesis  which  in  the 
case  of  a  single  chromatophore  are  centered  in  a  particular 
region  of  the  cell.  By  the  division  of  a  chromatophore  into 
numerous  plastids  the  photosynthetic  activities  are  distributed 
among  several  centers  and  a  much  better  balance  results  within 
the  cell.  It  is  very  interesting  that  the  large  elaborate  chroma- 
tophores  with  their  peculiar  internal  differentiations,  the  pyre- 


712  THE  AMERICAN  NATURALIST.        [Vou  XXXIX. 

noids  and  caryoids,  should  have  been  displaced  by  the  much 
simpler  and  apparently  homogeneous  plastids. 

A  comparative  study  of  chromatophores  and  plastids  from 
the  point  of  view  of  their  evolutionary  history  is  much  to  be 
desired  and  such  research  would  necessitate  extensive  studies 
among  the  lower  groups  of  algae  and  especially  in  the  Proto- 
coccales.  Such  studies  would  involve  far  more  than  the  general 
morphology  of  the  chromatophore  and  plastid.  The  structure 
and  activities  of  the  pyrenoid  are  a  very  important  subject  as 
shown  by  the  investigations  of  Timberlake  on  Hydrodictyon 
and  nothing  is  known  of  the  function  of  the  caryoid.  A  de- 
tailed investigation  of  the  chromatophore  or  plastid  throughout 
ontogeny  is  yet  to  be  made. 

The  Cytoplasm. —  There  is  no  region  of  the  plant  cell  whose 
structure  is  more  varied  and  as  little  understood  as  that  pre- 
sented by  the  cytoplasm  with  its  diverse  conditions.  We  have 
throughout  these  papers  held  to  the  classification  of  Strasburger 
that  the  cytoplasm  may  be  separated  into  two  forms :  kinoplasm 
and  trophoplasm,  which  show  certain  structural  peculiarities  and 
are  characterized  by  very  different  forms  of  activity.  While  it 
must  be  acknowledged  that  kinoplasm  and  trophoplasm  are  very 
similar  in  certain  regions  of  the  cell  and  at  certain  periods  of 
the  cell  history,  still  the  distinctions  are  in  general  clearly 
marked. 

Kinoplasm  is  homogeneous  in  structure,  either  minutely 
granular  or  consisting  of  delicate  fibrillae  composed  of  very 
small  granules  placed  end  to  end.  The  homogeneous  condition 
is  characteristically  shown  in  the  three  forms  of  plasma  mem- 
branes which  cytoplasm  places  between  itself  and  external  or 
internal  surface  contacts.  The  three  membranes  are:  the  outer 
plasma  membrane,  the  nuclear  membrane,  and  the  vacuolar 
membranes.  They  are  certainly  closely  related  and  probably 
identical  in  structure  and  appear  to  be  the  natural  expression  of 
protoplasm  to  contact  with  a  fluid  (water)  medium.  The  fibril- 
lar  condition  appears  during  mitosis  and  serves  important  func- 
tions in  the  mechanism  (spindle)  through  which  the  chromosomes 
are  distributed  and  in  most  of  the  higher  plants  determines  the 
position  of  the  cell  wall  that  is  generally  formed  with  each 
nuclear  division. 


No.  466.]          STUDIES   ON  PLANT  CELL.— VIII.  713 

But  the  manifestations  of  kinoplasm  during  nuclear  division 
and  also  in  relation  to  cilia-bearing  surfaces  are  exceedingly 
various  and  it  is  among  these  structures  that  our  ignorance  of 
relationships  and  modes  of  origin  is  deepest.  These  kinoplasmic 
structures  have  been  described  in  various  connections  through- 
out this  series  of  papers  and  especially  in  Sections  I,  II,  and 
III,  and  need  not  be  treated  here.  But  the  point  which  should 
be  emphasized  in  this  connection  is  the  necessity  of  the  close 
study  of  their  simplest  expressions  in  the  lower  regions  of  the 
thallophytes.  The  most  varied  forms  of  kinoplasm  are  in  the 
thallophytes  where  asters,  centrospheres,  and  centrosomes  ob- 
tain and  where  ciliated  cells,  presumably  with  blepharoplasts, 
may  occupy  long  periods  of  the  life  history.  It  is  here  that  we 
must  search  for  information  that  will  bring  order  out  of  the  con- 
fusion of  our  present  accounts  and  insufficiency  of  knowledge. 
The  most  vital  problems  relating  to  kinoplasm  concern  the  ori- 
gin and  the  events  of  the  simplest  types  of  mitotic  phenomena 
and  the  formation  of  cilia.  We  have  a  fairly  clear  understand- 
ing of  the  general  features  of  mitosis  in  the  groups  above  the 
thallophytes  and  their  relation  to  the  lower  types  and  these  will 
be  briefly  treated  in  the  following  portion  of  this  section  under 
the  head  :  "  Some  Apparent  Tendencies  in  the  Evolution  of 
Mitotic  Phenomena."  But  the  events  of  mitosis  among  the 
thallophytes  are  exceedingly  various  and  difficult  to  understand 
and  nothing  is  known  of  their  origin  or  relation  to  the  simpler 
conditions  which  must  be  present  in  the  lowest  regions  of  the 
Chlorophyceae  and  in  the  Cyanophyceae. 

Trophoplasm  comprises  all  of  the  cytoplasm  included  within 
the  plasma  membranes.  While  this  region  does  not  give  rise  to 
such  highly  differentiated  cell  organs  as  the  kinoplasm,  never- 
theless some  remarkably  interesting  structures  are  developed. 
Coenocentra  and  Physodes  are  specialized  structures  of  exceed- 
ing interest  and  our  ignorance  of  the  latter  is  truly  remarkable. 
Nematocysts  if  trophoplasmic  offer  another  attractive  subject  for 
investigation.  In  a  sense,  chromatophores  and  plastids  may  be 
considered  trophoplasmic  but  their  high  grade  of  specialization 
and  fixity  as  cell  organs  gives  them  a  certain  independence  of 
other  structures  in  the  cell.  Respecting  the  structure  of  the 


714  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

groundwork  of  trophoplasm,  whether  fibrillar,  granular,  or  pre- 
senting the  structure  of  foam,  botanical  science  has  as  yet  fur- 
nished very  little  systematic  study  and  this  field  of  research  is 
one  of  exceptional  opportunity  for  the  student  of  the  plant  cell. 

The  Cell  Wall. —  The  cell  wall  may  be  treated  from  two 
points  of  view  :  either  with  respect  to  the  strict  chemistry  of  its 
organization  and  development  or  more  largely  for  the  biological 
and  morphological  features  involved.  The  chemistry  of  the  cell 
wall  is  an  exceedingly  complex  subject  which  has  developed  a 
special  literature  of  its  own.  In  the  substance  termed  cellulose 
we  are  not  dealing  with  a  single  body  but  rather  with  a  large 
group  of  closely  related  bodies.  And  besides  the  members  of 
the  cellulose  group  there  may  be  present  foreign  substances  so 
intimately  associated  with  the  carbohydrates  as  to  resist  very 
severe  treatment.  We  cannot  even  touch  this  phase  of  the  sub- 
ject ;  a  brief  review  of  its  complexities  and  problems  is  presented 
by  Beer  (:  04)  and  there  are  further  references  in  Section  I  of 
these  "  Studies." 

There  are,  however,  some  biological  features  of  the  process  of 
wall  formation,  the  morphological  and  physiological  aspects  of 
the  phenomena  as  they  are  related  to  protoplasm,  which  offer 
some  exceedingly  interesting  problems  especially  among  the 
thallophytes.  It  has  long  been  a  matter  of  dispute  whether  the 
cell  wall  is  a  secretion  from  the  surface  of  a  plasma  membrane 
or  is  formed  wholly  or  in  part  by  the  transformation  of  such  a 
membrane. 

It  seems  to  be  established  now  that  substances  of  the  cellu- 
lose groups  are  only  formed  in  contact  with  plasma  membranes, 
that  is,  they  are  not  formed  actually  in  the  interior  of  proto- 
plasm although  they  may  appear  to  lie  in  such  situations.  Thus 
the  material  of  the  capillitium  of  the  Myxomycetes  which  is  of 
the  same  character  as  the  chief  substance  in  the  exterior  cover- 
ing of  the  fructification,  is  laid  down  within  vacuoles  in  the 
protoplasm,  and  is  therefore  in  contact  with  the  surface  of  vacu- 
olar  plasma  membranes  precisely  as  the  outer  covering  lies  in 
contact  with  the  surface  of  the  outer  plasma  membrane.  The 
morphological  relation  of  capillitium  and  outer  covering  to  the 
surface  of  plasma  membranes  is  therefore  precisely  the  same. 


No.  466.]          STUDIES  ON  PLANT  CELL.— VIII.  715 

And  similarly  the  cross  wall  which  takes  the  position  of  the  cell 
plate  at  the  end  of  mitosis  is  not  developed  from  the  transfor- 
mation of  a  film  of  protoplasm  but  is  laid  down  between  two 
surfaces  that  separate  to  form  a  thin  vacuole  which  later  spreads 
to  the  edge  of  the  cell  and  the  wall  is  deposited  between  these  two 
membranes  which  are  almost  in  contact.  There  are  a  number 
of  cases  in  which  large  strands  or  masses  of  protoplasm  have 
been  described  as  changing  directly  into  cellulose  but  it  is  prob- 
able that  these  examples  upon  further  study  will  exhibit  the 
same  relation  of  the  cellulose  substances  to  plasma  membranes 
as  in  the  typical  cases  of  wall  formation.  There  are  many  inter- 
esting examples  of  cellulose  formation  whose  precise  relation  to 
the  protoplasm  has  not  yet  been  determined. 

Respecting  the  exact  method  by  which  a  cellulose  wall  is  laid 
down  by  a  plasma  membrane  there  is  very  little  real  informa- 
tion. It  is  clear  now  that  the  cellulose  is  not  a  secretion  from 
the  plasma  membrane  comparable  to  a  mineral  shell.  There  is 
much  evidence  that  protoplasm  is  actually  sacrificed  in  the  de- 
velopment of  cellulose.  There  are  numerous  illustrations,  as  in 
the  tracheids  and  other  cells  empty  of  protoplasm,  where  the 
final  secondary  thickenings  are  deposited  as  the  protoplast  grows 
smaller  and  eventually  disappears,  a  large  part  of  its  substance 
evidently  contributing  to  the  deposits  which  are  members  of  the 
cellulose  group.  But  of  course  it  cannot  be  supposed  that  the 
molecules  of  the  proteids  are  changed  directly  into  those  of  the 
carbohydrates.  Nevertheless  it  does  seem  clear  that  the  carbo- 
hydrates appear  simultaneously  with  the  disappearance  of  the 
proteids  and  occupy  the  position  formerly  held  by  the  latter.  It 
is  probable  that  with  the  splitting  up  of  the  proteid  molecule, 
carbohydrate  material  is  formed  which  displaces  the  proteid  sub- 
stances. So  in  a  broad  sense  the  cellulose  deposit  actually  does 
represent  a  transformation  of  a  plasma  membrane. 

The  evidence  in  general  favors  the  view  that  the  wall,  lamellae, 
and  other  deposits  of  cellulose  only  increase  in  amount  when  in 
actual  contact  with  a  plasma  membrane.  Some  apparent  excep- 
tions to  this  principle  are  easily  understood.  Thus  cell  walls  or 
portions  of  such  may  swell  greatly  and  become  much  softer  in 
consistency  and  perhaps  even  mucilaginous.  There  are  no 


716  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

reasons  for  regarding  such  transformations  as  an  actual  increase 
in  the  carbohydrate  material  for  it  is  clear  that  the  substance  is 
a  body  with  a  greater  amount  of  water  in  its  organization  than 
is  present  in  the  more  usual  forms  of  cellulose  compounds. 
But  there  are  some  cases  which  are  not  so  easily  understood  and 
perhaps  the  most  widely  known  are  the  jnegaspore  walls  of  cer- 
tain species  of  Selaginella.  These  spores  are  remarkable  for  a 
differentiation  of  the  spore  wall  in  which  the  outer  layer  seems 
to  be  entirely  separated  from  the  inner  by  a  space  and  yet  is 
able  to  increase  enormously  in  size  and  take  on  marked  pecul- 
iarities of  structure,  but  apparently  without  any  relation  to  the 
protoplast.  It  may,  however,  be  justly  questioned  whether  the 
apparent  space  between  the  inner  and  outer  wall  is  really  a 
cavity  and  may  not  be  filled  with  plastic  material  which  holds 
the  two  walls  in  intimate  organic  relation  to  one  another  and  to 
the  protoplast.  Miss  Lyon  has  recently  given  this  subject  at- 
tention and  announced  her  belief  that  the  latter  condition  ob- 
tains. Her  conclusions  will  be  awaited  with  interest. 

As  regards  the  way  in  which  a  cell  wall  increases  in  size  we 
are  still  limited  to  the  two  conceptions  termed  ( i )  growth  by 
apposition  and  (2)  growth  by  intussusception.  The  first  method 
consists  in  the  laying  down  of  successive  layers  by  the  plasma 
membrane  and  results  in  a  thickening  of  the  cell  wall.  It  is  of 
course  a  comparatively  simple  process.  Growth  by  intussuscep- 
tion is  a  stretching  or  expansion  of  the  substance  which  seems 
to  be  greatly  increased  in  quantity  although  the  morphology  of 
the  structure  remains  the  same.  The  current  explanation  out- 
lined by  Nageli  assumes  that  new  molecules  of  carbohydrates 
are  intercalated  among  the  old.  It  seems  more  probable  that 
the  increase  in  bulk  is  due  to  some  modification  or  rearrange- 
ment of  existing  molecules,  involved,  perhaps  with  an  increase 
of  material  but  not  through  the  actual  intercalation  of  new 
molecules  of  the  same  or  original  carbohydrates.  The  chem- 
istry of  the  carbohydrates  is  so  complex  that  great  changes  of 
form,  bulk,  or  optical  properties  may  be  readily  assumed  which 
would  quite  change  the  appearance  of  a  structure  without,  how- 
ever, necessitating  the  transportation  of  new  carbohydrate  sub- 
stance to  it  directly. 


No.  466.]          STUDIES   ON  PLANT  CELL.— VIII.  717 

There  are  many  forms,  particularly  among  the  lower  plants, 
where  studies  on  the  processes  of  wall  formation  are  sure  to 
throw  much  light  on  the  fundamental  problems  which  we  have 
discussed.  And  a  particularly  interesting  study  might  be  made 
of  the  evolutionary  history  of  the  cell  wall  among  the  thallo- 
phytes  and  in  the  modifications  introduced  when  plants  pass 
from  aquatic  habits  to  aerial  or  terrestrial  conditions.  Our 
attention  has  been  chiefly  centered  on  the  structure  of  the  pro- 
toplast and  the  morphology  and  behavior  of  its  parts.  We  are 
likely  soon  to  give  more  study  to  the  carbohydrate  membranes 
and  walls  and  this  subject  is  likely  to  be  very  fruitful  for  inves- 
tigation. 

3.     SOME  APPARENT  TENDENCIES  IN  THE  EVOLUTION  OF 
MITOTIC  PHENOMENA. 

Our  brief  descriptions  in  Section  II  (Amer.  Nat.,  vol.  38,  p. 
431,  June,  1904)  of  the  various  kinoplasmic  structures  developed 
during  mitosis  in  different  groups  of  plants  brings  up  the  prob- 
lem in  their  relationships  to  one  another,  i.  e.,  the  evolutionary 
tendencies  in  the  differentiation  of  mitotic  phenomena.  We 
have  seen  that  the  thallophytes  present  an  especially  diverse 
assortment  of  kinoplasmic  structures  associated  with  the  spindle 
and  its  method  of  development.  The  spindle  fibers,  whether 
formed  within  the  nuclear  membrane  (intranuclear)  or  arising 
from  without  (extranuclear),  are  associated  with  centrosomes  or 
centrospheres  to  form  asters  in  a  number  of  well  known  types 
as  Stypocaulon,  Dictyota,  Fucus,  Corallina,  certain  diatoms,  the 
ascus,  and  the  basidium.  Centrospheres  are  found  in  certain 
phases  of  the  life  history  of  liverworts  as  in  the  germinating 
spore  of  Pellia.  A  second  type  of  kinoplasmic  structure  resem- 
bling in  certain  features  the  aster  but  with  some  fundamental 
differences  has  been  termed  the  polar  cap.  The  polar  cap  is  an 
ill  denned  region  of  kinoplasm,  generally  larger  than  a  centre- 
sphere  and  without  clear  boundaries,  which  forms  a  region  for 
the  insertion  of  spindle  fibers.  Polar  caps  are  well  illustrated 
in  the  mitoses  of  vegetative  tissues  and  meristematic  regions, 
especially  among  the  higher  plants  (pteridophytes  and  sperma- 


718  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

tophytes).  They  sometimes  approach  the  centrosphere  very 
closely  in  their  morphology. 

The  third  and  highest  type  of  spindle  formation  in  plants  is 
that  illustrated  in  the  mitoses  within  the  spore  mother-cell  which 
were  given  special  treatment  in  Section  III  (Amer.  Nat.,  vol.  38, 
p.  725,  October,  1904).  In  this  remarkable  cell  the  spindles 
develop  from  a  mesh  of  independent  fibrillae  which  at  prophase 
more  or  less  completely  surround  the  nucleus.  The  poles  of 
the  spindle  arise  by  the  grouping  of  cones  of  fibrillae  so  that  a 
single  axis  is  finally  established  but  without  any  kinoplasmic  cen- 
ters at  the  poles.  This  type  of  spindle  formation  which  may  be 
termed  the  free  fibrillar  type  is  one  of  the  most  interesting 
cytological  peculiarities  of  plants.  It  has  been  found  in  all 
types  whose  sporophytic  phase  terminates  its  history  with  a 
spore  mother-cell,  although  the  accounts  in  the  Hepaticae  are 
not  in  full  accord. 

Is  it  possible  to  connect  the  various  types  of  spindle  formation 
with  one  another  and  to  establish  any  evolutionary  tendencies  in 
the  processes  involved  ;  and  have  the  different  manifestations  of 
kinoplasm  such  as  centrosomes,  centrospheres,  polar  caps,  free 
fibrillar  condition,  and  the  mysterious  structure  called  the  ble- 
pharoplast  any  genetic  relation  to  one  another  ?  The  confusion 
is  so  great  among  the  thallophytes  that  the  author  sees  little 
hope  at  present  of  establishing  clearly  any  relationships  between 
the  types  of  centrospheres  and  centrosomes  with  their  systems 
of  radiations  (asters)  and  we  must  patiently  wait  for  more  infor- 
mation. And  respecting  the  origin  of  these  structures  from  the 
simpler  types  of  mitosis  we  are  absolutely  in  the  dark.  But 
the  relation  which  polar  caps  and  the  free  fibrillar  type  of  spin- 
dle formation  bear  to  centrospheres  is  less  perplexing  and  it 
seems  possible  to  define  certain  common  features  among  these 
structures  which  hold  them  together  with  a  degree  of  unity  in 
their  relations  to  mitosis.  That  phase  of  the  subject  will  be 
considered  in  this  treatment.  The  Hepaticae  as  a  group  occupy 
an  interesting  position  with  respect  to  the  character  of  mitotic 
phenomena  at  various  periods  of  ontogeny,  between  conditions 
in  the  pteridophytes,  which  are  obviously  similar  to  the  sperma- 
tophytes,  and  conditions  in  the  thallophytes.  This  was  brought 


No.  466.]          STUDIES   ON  PLANT  CELL.—  VIII.  719 

out  by  the  work  of  Farmer  whose  accounts  of  centrosomes  and 
centrospheres  in  the  germinating  spores  of  Pellia  and  within 
the  spore  mother-cell  of  various  liverworts,  together-  with  his 
account  of  a  "  quadripolar  spindle  ' '  made  it  evident  that  the 
group  offered  some  very  interesting  cytological  problems.  They 
led  the  author  to  the  study  Anthoceros  (Davis,  '99)  and  Pellia 
(Davis,  :oi),  investigations  which  have  been  followed  by  Van 
Hook  (:  oo)  on  Marchantia  and  Anthoceros,  Moore  (:  03)  on 
Pallavicinia,  Chamberlain  (:  03)  and  Gregoire  and  Berghs  (:O4) 
on  Pellia,  while  Ikeno  (:  03)  has  studied  the  processes  of  sperma- 
togenesis  in  Marchantia. 

My  studies  on  sporogenesis  in  Anthoceros  and  Pellia  led  me 
to  conclude  that  the  processes  of  spindle  formation  did  not 
differ  in  any  essentials  from  those  in  the  pteridophytes  and  sper- 
matophytes.  There  are  present  two  successive  mitoses  and  the 
spindles  are  formed  from  a  surrounding  mesh  of  fibrillae  devel- 
oped from  the  kinoplasm  associated  with  the  nuclear  membrane 
and  without  achromatic  centers  (centrospheres  or  centrosomes). 
They  exhibit  clearly  the  free  fibrillar  type  of  spindle  formation 
although  in  somewhat  simpler  form  than  in  the  pteridophytes 
and  spermatophytes.  The  poles  of  the  spindles  generally  end 
bluntly  in  areas  of  granular  kinoplasm  but  these  seem  to  me  too 
indefinite  in  form  to  deserve  the  designation  of  centrospheres 
and  such  granular  inclusions  as  may  be  present  are  too  variable 
in  number  and  position  to  be  termed  centrosomes.  There  is 
clearly  present  in  Pellia  during  the  prophase  of  the  first  mitosis 
a  four-rayed  achromatic  structure  which  is  later  replaced  by  a 
typical  bipolar  spindle.  This  four-rayed  kinoplasmic  structure 
is  evidently  the  same  as  Farmer's  "  quadripolar  spindle  "  which 
he  described  as  associated  with  a  simultaneous  distribution  of  the 
chromatin  in  Pallavicinia  to  form  at  once  four  daughter  nuclei. 
I  was  led  to  doubt  this  account  and  to  suggest  that  the  "quad- 
ripolar spindle "  might  prove  to  be  simply  a  phenomenon  of 
prophase  associated  with  the  peculiar  four-lobed  structure  of 
the  spore  mother-cell  in  the  Jungermanniales.  I  stated  my 
belief  that  the  distribution  of  the  chromosomes  during  sporo- 
genesis in  all  liverworts  would  be  found  to  take  place  through 
two  successive  mitoses  after  the  usual  manner.  Moore  (:  03) 


720  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

has  recently  studied  an  American  species  of  Pallavicinia  and 
has  failed  to  confirm  Farmer's  conclusions.  He  found  the  four- 
rayed  figure,  which  Farmer  terms  a  "  quadripolar  spindle,"  a 
conspicuous  feature  of  the  first  mitosis  here  as  in  Pellia  but 
there  was  no  indication  of  a  simultaneous  distribution  of  quad- 
rupled chromosomes  to  form  four  daughter  nuclei  as  reported 
by  Farmer.  The  four-rayed  figure  was  merely  preliminary  to 
the  first  mitosis  whose  spindle  at  metaphase  was  bipolar  and  the 
first  mitosis  was  followed  shortly  by  a  second,  so  that  Pallavi- 
cinia offers  no  exception  to  the  essential  features  of  sporogenesis 
as  known  in  all  groups  above  the  thallophytes. 

Farmer  (Bot.  Gaz.,  vol.  37,  p.  63,  1904)  has  taken  exception 
to  the  restriction  of  the  term  spindle  by  Moore  and  myself  to 
the  structure  found  at  metaphase  and  holds  that  the  four-rayed 
structure  is  a  part  of  the  spindle  apparatus.  In  this  discussion 
he  appears  to  avoid  the  issue,  which  is  not  the  broader  or  nar- 
rower application  of  the  term  spindle,  a  mere  matter  of  usage, 
but  concerns  the  fundamental  character  of  the  mitoses  during 
sporogenesis  whether  they  are  two  in  number  and  successive  in 
all  forms  or  whether  Pallavicinia  presents  an  extraordinary  ex- 
ception in  a  distribution  of  the  chromatin  to  form  four  daughter 
nuclei  simultaneously  in  the  spore  mother-cell.  Farmer  (:  05) 
has  recently  reaffirmed  his  view  that  the  poles  of  the  four-rayed 
figure  in  Aneura  and  presumably  in  other  Jungermanniales  are 
occupied  by  centrospheres  and  that  sometimes  a  central  body 
(centrosomes)  may  be  distinguished  in  each.  This  statement 
involves  again  a  matter  of  usage  in  which  I  should  differ  from 
Farmer  for  my  studies  and  those  of  Moore  do  not  seem  to  me 
to  justify  the  application  of  these  terms  to  regions  of  kinoplasm 
whose  form  is  so  ill  defined  and  history  so  transient  within  the 
cell. 

These  disputed  points  which  were  also  discussed  in  Section 
III  (Amer.  Nat..,  vol.  38,  pp.  727-732,  October,  1904)  are  of 
importance  in  relation  to  the  mitotic  phenomena  in  other  periods 
of  the  life  history  of  liverworts  which  will  now  be  considered. 
It  may  be  stated,  however,  that  other  investigators  who  have 
studied  the  processes  of  sporogenesis  in  the  liverworts  (Van 
Hook,  :  oo  ;  Chamberlain,  :  03  ;  Gregoire  and  Berghs,  :  04)  sup- 


No.  466.]          STUDIES   ON   PLANT  CELL.—  VIII.  721 

port  my  general  program  of  sporogenesis  with  the  free  fibrillar 
type  of  spindle  formation.  There  seems  to  be  little  question 
but  that  centrospheres  are  present  and  conspicuous  in  the  early 
mitoses  within  the  spore  of  Pellia.  They  have  been  especially 
studied  by  Farmer  and  Reeves  ('94),  Davis  (:oi),  Chamberlain 
(:O3),  and  Gregoire  and  Berghs  (:O4).  All  of  these  authors 
have  agreed  that  asters  are  clearly  defined  in  the  early  mitoses 
within  the  spore  and  most  of  them  have  termed  the  region  of 
kinoplasm  in  the  center  of  the  aster  a  centrosphere.  The  struc- 
tures are  less  prominent  in  the  third  mitosis  and  are  perhaps 
replaced  in  later  periods  of  the  gametophyte  history  by  kino- 
plasmic  polar  caps.  Polar  caps  are  characteristic  of  the  mitoses 
in  the  seta  of  Pellia  (Davis,  :oi).  However,  Van  Hook  has 
described  centrospheres  with  radiations  at  the  poles  of  the 
spindles  of  the  archegoniophores  of  Marchantia,  whose  centers 
sometimes  contained  centrosomes,  and  it  is  possible  that  the 
centrosphere  runs  through  a  considerable  period  in  the  life  his- 
tory of  liverworts.  There  is  complete  agreement  that  the  cen- 
trospheres when  present  arise  de  novo  and  independently  of  one 
another  during  the  prophase  of  mitosis  and  that  they  disappear  at 
telophase.  Ikeno  has,  however,  described  centrosomes  during 
the  mitoses  within  the  antheridium  which  are  said  to  divide  and 
pass  to  opposite  sides  of  the  nucleus  where  they  become  the 
poles  of  the  spindles.  They  cannot  be  found  after  the  mitosis  is 
completed,  but  are  described  as  formed  de  novo  in  the  interior 
of  the  nucleus  and  thrust  through  the  nuclear  membrane  into 
the  cytoplasm  previous  to  each  mitosis.  After  the  final  divi- 
sion in  the  antheridium,  the  centrosome  remains  to  function 
as  a  blepharoplast. 

Thus  we  see  that  the  liverworts  present  during  their  life 
history  an  almost  complete  range  of  kinoplasmic  structures 
associated  with  the  nuclear  divisions  from  centrosomes  and  cen- 
trospheres to  polar  caps  and  that  type  of  spindle  formation 
characterized  by  free  fibrillae  gathered  into  cones  but  entirely 
independent  of  definitely  organized  centers.  There  is  also  pres- 
ent the  blepharoplast.  I  emphasized  this  range  of  kinoplasmic 
structure  in  my  paper  on  Pellia  and  it  seemed  to  me  one  of  the 
most  interesting  features  of  the  liverworts.  In  this  paper 


722  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

(Davis,  :oi,  p.  171)  are  outlined  the  changes  in  form  which 
kinoplasm  may  assume  in  the  mitoses  of  the  liverworts  upon 
which  is  based  a  theory  of  a  cycle  through  which  kinoplasm 
may  run  in  the  history  of  a  cell.  On  this  theory,  centrosphere, 
polar  cap,  and  the  free  fibrillar  condition  are  all  secondary  devel- 
opments from  a  primal  finely  granular  kinoplasm  which  is  the 
only  form  of  kinoplasm  that  is  in  any  sense  permanent  in  the 
cell.  This  finely  granular  kinoplasm  is  always  present  in  char- 
acteristic form  in  the  plasma  membranes  of  the  cell.  The  sub- 
stance of  centrospheres,  polar  caps,  and  fibrillae  arises  from 
accumulations  of  granular  kinoplasm  during  prophase  and  these 
structures  return  to  the  same  undifferentiated  granular  kino- 
plasm at  the  end  of  mitosis  or  become  lost  in  the  general 
cytoplasm  of  the  cell. 

The  cycle  is  from  an  undifferentiated  finely  granular  kino- 
plasm through  certain  specialized  conditions  either  wholly  or 
in  part  fibrillar  in  structure  back  to  the  granular  state.  The 
centrosphere  and  polar  cap  are  regions  from  which  fibrillae  de- 
velop at  least  in  part  and  to  which  they  may  remain  attached  as 
to  an  anchorage.  The  polar  cap  is  a  less  clearly  differentiated 
kinoplasmic  center  than  the  centrosphere  but  does  not  differ 
from  it  in  the  essentials  of  its  organization.  It  seems  to  me  that 
the  two  structures  are  very  closely  related  in  the  liverworts  and 
that  in  this  group  we  may  readily  conceive  the  polar  cap  as  de- 
rived from  the  centrosphere.  The  'free  fibrillar  type  of  spindle 
formation  is  a  step  farther  in  the  direction  of  such  a  distribution 
of  the  kinoplasm  that  no  very  positive  centers  for  the  develop- 
ment of  the  spindles  may  be  distinguished.  The  four-rayed 
structure  (quadripolar  spindle)  so  characteristic  of  the  spore 
mother-cell  in  the  Jungermanniales  represents  a  group  of  four 
temporary  centers  for  the  formation  of  fibrillae  and  there  is 
clearly  a  gathering  of  kinoplasm  at  these  points  but  the  regions 
are  so  vague  in  outline  as  hardly  to  justify  the  designation  of 
centrospheres.  From  the  fibrillar  state,  kinoplasm  returns  to 
the  finely  granular  condition  by  the  contraction  of  the  fibers 
which  thus  contribute  their  substance  to  some  common  area. 
The  area  may  lie  around  the  chromosomes  of  the  daughter 
nuclei  where  it  becomes  later  in  part  at  least  a  nuclear  mem- 


No.  466.]  STUDIES   ON  PLANT  CELL.  — VIII.  723 

brane.  Or  the  area  may  be  a  cell  plate  whose  halves  on  division 
finally  merge  with  outer  plasma  membranes  of  the  cells.  The 
spindle  fibers  which  cut  out  the  spore  areas  in  the-ascus  form 
the  basis  of  a  plasma  membrane.  Thus  the  fate  of  all  kinoplas- 
mic  fibrillae  seems  to  be  a  final  return  to  the  undifferentiated, 
finely  granular  condition  so  characteristic  of  plasma  membranes 
which  according  to  this  theory  is  the  condition  from  which  they 
arose. 

Thus  I  believe  the  liverworts  present  rather  striking  evidence 
of  a  relationship  between  the  centrosphere,  polar  cap,  and  the 
free  fibrillar  condition  of  spindle  formation  and  establish  an 
evolutionary  tendency  from  the  first  two  types  of  kinoplasmic 
differentiation  towards  the  latter.  The  free  fibrillar  type  of 
spindle  formation  is  found  in  a  very  simple  form  in  this  group, 
sometimes  with  temporary  centers,  as  in  the  four-rayed  figure 
(quadripolar  spindle)  of  prophase,  whose  poles  have  accumula- 
tions of  kinoplasm  in  the  position  of  centrospheres.  The  polar 
caps  are  likely  to  prove  a  much  simplified  type  of  centrosphere 
whose  kinoplasm  is  no  longer  gathered  to  form  conspicuous 
spherical  centers.  With  respect  to  the  problem  of  the  homol- 
ogies  and  nature  of  the  blepharoplast,  the  liverworts  furnish  as 
yet  no  material  assistance  and  this  structure  stands  at  present 
as  one  of  the  most  interesting  puzzles  of  plant  cytology.  As 
stated  in  the  beginning,  the  variety  of  centrosomes  and  centro- 
spheres with  and  without  radiations  in  various  types  of  the  thal- 
lophytes  seems  to  me  too  confusing  to  promise  an  understanding 
of  their  relationships  at  present. 

Gregoire  and  Berghs  (:  04)  have  interpreted  the  structure  of 
the  mitotic  figure  in  the  germinating  spore  of  Pellia  in  a  very 
different  manner  from  the  accounts  of  Farmer,  Chamberlain, 
and  myself.  They  consider  the  asters  to  arise  through  a  re- 
arrangement of  the  cytoplasmic  network  around  the  nucleus. 
They  affirm  that  there  are  no  true  centrospheres  nor  any  ac- 
cumulations of  granular  kinoplasm  to  constitute  the  centers  of 
origin  for  the  spindle  fibers  or  the  radiations  around  the  poles  of 
the  spindle.  The  centers  of  the  asters  ("vesicules  polaires  ") 
are  said  to  have  a  vesicular  structure  and  neither  they  nor  the 
nucleus  contributes  to  the  building  up  of  the  spindle  which  is 


724  THE   AMERICAN  NATURALIST.         [VOL.  XXXIX. 

developed  entirely  out  of  the  cytoplasmic  network.  The  au- 
thors are  unable  to  distinguish  a  kinoplasm  distinct  from  the 
general  network  of  the  cell.  These  are  vital  points  of  differ- 
ence which  are  fundamental  to  the  understanding  of  mitotic 
phenomena  and  rest  of  course  on  matters  of  fact.  The  chief 
points  at  issue  concern  the  structure  and  development  of  the 
asters  and  the  nature  of  the  material  at  their  centers.  My  own 
studies  and  those  of  Farmer  and  Chamberlain  have  convinced 
me  that  there  is  an  accumulation  of  substance  (kinoplasm)  in 
the  centers  of  the  asters  and  polar  caps  to  such  an  amount  that 
it  must  be  regarded  as  a  definite  structure  in  the  cell  and  its 
morphology  and  relations  to  the  spindle  have  certainly  justified 
us  in  considering  it  as  similar  to  the  centrosphere  of  the  thallo- 
phytes. 

4.    THE    ESSENTIAL    STRUCTURES  IN  THE    PLANT    CELL    AND 
THEIR  BEHAVIOR  IN  ONTOGENY. 

The  cell  is  composed  of  a  series  of  osmotic  membranes  be- 
tween which  are  included  a  number  of  protoplasmic  structures 
whose  morphology  and  minute  organization  is  various.  They 
are  :  the  outer  plasma,  the  vacuolar,  and  the  nuclear  membranes. 
Each  of  these  sustains  a  relation  to  some  fluid  which  bathes  its 
surface.  The  fluid  nature  of  the  nuclear  sap  and  cell  sap  is 
obvious  but  the  outer  plasma  membrane  is  also  against  a  moist 
surface  since  the  cell  walls  of  tissues  are  normally  saturated  with 
water.  The  structure  of  the  plasma  membranes  is  apparently 
the  same.  They  consist  of  the  homogeneous  finely  gran- 
ular protoplasm  that  is  designated  kinoplasm.  The  protoplas- 
mic structures  included  within  the  plasma  membranes  may  be 
grouped  as  cytoplasmic  and  nuclear.  The  greater  part  of  the 
cytoplasm,  including  that  which  is  termed  trophoplasm,  has  an 
organization  peculiar  to  itself  and  very  different  from  that  of 
the  plasma  membranes.  This  structure  has  been  described  as 
alveolar  or  of  the  nature  of  foam  and  sometimes  fibrillar  and 
with  various  large  granular  inclusions.  The  cytoplasm  also  con- 
tains the  characteristic  organs  termed  plastids.  The  conspicu- 
ous structures  of  the  nucleus  are :  the  chromatic  elements 


No.  466.]  STUDIES   ON  PLANT  CELL.— VIII.  725 

appearing  as  chromosomes  during  mitosis  and  the  nucleoli. 
These  structures  are  so  easily  recognized  and  play  such  impor- 
tant parts  in  the  events  of  nuclear  division  that  they  command 
attention  at  once  as  the  essential  elements  in  the  nucleus.  The 
nucleus  may  also  contain  other  material  such  as  linin  which, 
however,  does  not  seem  to  have  a  fixed  form  or  behavior  in  the 
cell.  Finally  there  are  certain  kinoplasmic  structures,  as  cen- 
trosomes,  centrospheres,  and  blepharoplasts,  whose  behavior 
throughout  cell  history  has  been  much  discussed.  We  shall  now 
consider  the  most  important  of  these  structures,  those  which 
seem  essential  to  the  cell  in  ontogeny. 

The  outer  plasma  membrane  naturally  retains  its  morphologi- 
cal entity  throughout  all  cell  divisions  with  such  slight  changes 
as  when  new  parts  are  intercalated  into  its  area  through  the 
vacuoles  that  are  utilized  in  the  segmentation  of  protoplasm. 
Vacuolar  membranes  are  constantly  shifting  and  cannot  be  fol- 
lowed during  cell  division  excepting  in  such  cells  as  have  one 
large  central  vacuole  (the  tonoplast  of  De  Vries).  Such  a  cen- 
tral vacuole  is  much  more  characteristic  of  old  cells  and  tissues 
than  of  young  or  embryonic  regions.  There  is  certainly  no 
reason  to  suppose  that  it  has  organic  existence  through  any  very 
extended  period  of  the  life  history.  The  nuclear  membrane 
becomes  lost  during  the  prophase  of  mitosis  and  there  is  .much 
evidence  that  its  kinoplasm  contributes  in  some  cases  to  the 
formation  of  spindle  fibers.  Thus  the  nuclear  membrane  disap- 
pears as  a  structure  in  the  cell  during  mitosis  and  new  vacuoles 
are  formed  around  the  assemblages  of  daughter  chromosomes 
during  telophase,  leading  of  course  to  the  formation  of  fresh 
nuclear  membranes  at  their  surface  of  contact  with  the  sur- 
rounding cytoplasm. 

There  is  perhaps  no  region  of  the  cell  protoplast  that  presents 
such  different  appearances  through  long  periods  of  the  cell  -his- 
tory as  the  trophoplasm.  This  is  largely  due  to  the  varying 
character  of  the  inclusions  which  are  not  in  themselves  proto- 
plasmic but  which  give  a  mixed  structure  to  the  trophoplasmic 
regions  of  the  cell.  The  inclusions  may  be  carbohydrate  or  pro- 
teid  bodies  held  within  spaces  in  the  trophoplasmic  groundwork 
or  they  may  be  globules  of  oil  or  fatty  substances.  These 


726  THE  AMERICAN  NATURALIST.       [You  XXXIX. 

inclusions  occupy  small  spaces  in  the  trophoplasm  which  are 
essentially  vacuoles.  There  is  also  a  class  of  granular  inclusions 
of  a  proteid  nature  which  probably  represent  material  in  very 
close  organic  relation  to  the  substance  of  protoplasm.  Tropho- 
plasm does  not  then  have  so  clearly  denned  a  type  of  structure 
as  do  the  other  regions  of  the  protoplast  but  it  is  hardly  probable 
that  its  essential  nature  changes  very  materially  throughout  the 
life  history.  The  organization  of  trophoplasm  is  itself  a  matter 
of  dispute  but  the  prevailing  views  favor  an  alveolar  or  foam 
structure  with  a  fibrous  character  at  times  somewhat  resembling 
the  texture  of  sponge. 

Ever  since  the  classical  investigations  of  Schimper  upon  the 
plastid  it  has  generally  been  held  that  these  structures  are  per- 
manent organs  of  the  cell,  reproducing  by  fission,  and  carried 
along  from  one  cell  generation  to  the  next  with  as  much  per- 
manence as  the  nucleus.  Schimper  discovered  plastids  in  the 
oospheres  of  certain  spermatophytes  and  in  a  variety  of  embry- 
onic tissues  and  concluded  that  the  structures  passed  from 
parents  to  offspring  as  leucoplasts  when  no  trace  of  color  could 
be  found  in  the  reproductive  cells  or  embryonic  tissues.  There 
has  been,  however,  no  systematic  study  of  the  plastid  through- 
out the  life  history  of  higher  plants  and  in  most  of  the  green 
thallophytes  there  are  reproductive  phases,  such  as  resting 
spores,  where  we  have  no  knowledge  of  the  structure  or  distri- 
bution of  the  chromatophores  in  the  cell.  It  is  very  important 
that  the  plastid  be  investigated  with  the  same  degree  of  atten- 
tion which  has  been  given  to  the  nucleus,  and  that  it  be  fol- 
lowed through  all  periods  of  the  life  history  in  forms  where  the 
color  becomes  greatly  modified  or  is  absent  in  the  reproductive 
cells  and  embryonic  (meristematic)  regions  of  the  plant.  Any- 
one who  has  studied  the  embryonic  tissues  of  plants  will  realize 
the  difficulties  of  the  investigation  which  will  probably  involve 
the  development  of  methods  of  technique,  especially  of  staining, 
somewhat  different  from  those  generally  employed  in  cell 
studies. 

We  may  now  consider  the  elements  in  the  nucleus  and  their 
behavior  during  ontogeny.  This  is  one  of  the  most  interesting 
subjects  in  cell  studies,  for  the  importance  of  the  chromosomes 


No.  466.]          STUDIES   ON  PLANT  CELL.—  VIII.  727 

and  chromosome  history  in  relation  to  problems  of  development, 
heredity,  hybridization,  and  variation  is  clearly  understood,  and 
these  subjects  have  already  been  treated  in  Section  V,  "  Cell 
Activities  at  Critical  Periods  of  Ontogeny  in  Plants."  Also 
some  recent  papers  on  the  nucleolus  of  which  Wager's  (:  04)  is 
the  most  comprehensive,  have  brought  this  structure  into  very 
close  relation  with  the  chromatin  content  of  the  nucleus,  and  the 
nucleolus  must  now  be  considered  in  any  treatment  of  the  chro- 
mosomes. The  problems  hinge  on  what  is  termed  the  individu- 
ality of  the  chromosome,  which  is  the  question  whether  or  not 
the  chromosome  is  a  structural  entity  maintaining  its  independ- 
ence completely  through  each  and  all  of  the  cell  divisions  in  a 
life  history.  There  is  also  involved  the  view  that  the  chromo- 
somes have  come  down  from  a  line  of  ancestral  structures, 
reproducing  by  fission  in  every  mitosis  throughout  the  history 
of  the  race. 

There  are  two  extremes  in  the  views  on  this  exceedingly 
interesting  conception  and  also  an  intermediate  position.  The 
one  extreme  has  recently  been  set  forth  by  Boveri  (:  04)  in  a 
very  clear  statement.  This  view  regards  the  chromosomes  as 
structural  entities,  possibly  elementary  organisms,  which  main- 
tain an  organic  individuality  and  independent  existence  in  the 
cell.  They  are  further  regarded  as  in  their  typical  form  when 
present  as  rods  or  short  filaments  during  mitosis.  Their  be- 
havior in  the  resting  nucleus  is  one  of  great  metabolic  activity 
which  affects  their  morphology  for  the  time  being. 

Those  who  are  inclined  to  doubt  the  individuality  of  the  chro- 
mosomes and  to  hold  off  from  a  full  acceptance  of  the  theory, 
base  their  attitude  on  the  extreme  difficulty  or  perhaps  impossi- 
bility of  following  the  chromosomes  as  entities  through  the  rest- 
ing nucleus  from  one  mitosis  to  another.  These  difficulties  are 
well  known  to  those  who  have  studied  chromosomes  even  in 
nuclei  which  are  most  favorable  for  the  investigation  of  their 
morphology.  The  chromosomes  which  enter  the  daughter 
nuclei  from  a  mitosis  generally  lose  their  form  and  the  chroma- 
tin  becomes  so  distributed  on  a  linin  network  or  in  a  nucleolar 
structure  that  the  outlines  of  the  original  structures  become 
quite  lost.  Mottier  (:  03)  in  his  recent  studies  on  the  spore 


728  THE   AMERICAN  NATURALIST.      [VOL.  XXXIX. 

mother-cell  of  certain  angiosperms  has  emphasized  these  points 
and  Gre^goire  and  Wygaerts  (:  03)  have  also  shown  the  difficul- 
ties of  following  the  chromosomes  in  the  resting  nuclei  of  the 
root  tip  and  spore  mother-cell  of  Trillium,  stating  that  the  struc- 
tures become  resolved  into  an  alveolar  network. 

On  the  other  hand  Rosenberg  (:  04)  claims  that  the  chromo- 
somes may  be  clearly  recognized  in  the  resting  nuclei  of  some 
forms  and  cites  Capsella  bursa-pastoris  as  a  particularly  good 
illustration.  In  this  plant  the  chromosomes  are  described  as 
small  granular  bodies  scattered  throughout  the  nucleus  in  fixed 
number  at  various  stages  of  ontogeny.  Thus  there  are  16  in 
cells  of  the  garnet ophyte  and  32  in  those  of  the  sporophyte 
while  48  of  these  bodies  were  counted  in  the  nuclei  of  the  endo- 
sperm as  would  be  expected  if  these  nuclei  are  descendants  of  a 
triple  fusion  in  the  embryo-sac.  Similar  conditions  are  reported 
in  other  forms  and  there  is  considerable  evidence  giving  weight 
to  the  view  that  chromosomes  may  be  actually  followed  through 
all  periods  of  the  nuclear  history  in  some  favorable  types. 

Apart  from  the  actual  demonstration  of  the  chromosomes  in 
the  resting  nuclei  and  their  recognition  as  structural  entities 
through  successive  cell  divisions  there  is  much  general  evidence 
in  support  of  the  theory  of  the  individuality  of  the  chromosomes. 
This  evidence  lies  in  the  nuclear  fusions  of  fertilization  and  the 
mitoses  of  processes  of  segmentation  that  follow  where  the 
chromosomes  are  known  to  remain  separate  and  have  been  dis- 
tinguished as  maternal  and  paternal.  Also,  as  we  have  seen 
from  the  discussions  of  reduction  phenomena  at  sporogenesis 
and  the  behavior  of  the  chromosomes  in  hybridization,  there  are 
good  reasons  for  believing  that  maternal  and  paternal  chromo- 
somes remain  separate  all  through  the  sporophyte  generation 
and  are  distributed  to  the  offspring  during  sporogenesis.  The 
importance  of  these  events  in  the  minds  of  all  investigators  has 
rested  very  largely  on  the  behavior  of  the  chromosomes  and  has 
led  to  the  very  gener'al  assumption  that  they  must  stand  for 
units  of  organization  and  may  be  counted  as  constant  factors  in 
the  problems  of  heredity.  It  is  not  necessary  to  adopt  Boveri's 
extreme  views  to  hold  still  the  theory  of  the  individuality  of  the 
chromosomes.  Nor  is  it  necessary  to  assume  that  the  structures 


No.  466.]  STUDIES   ON  PLANT  CELL.  — VIII.  729 

have  a  distinct  organization  which  holds  throughout  the  life  his- 
tory. The  form  of  the  chromosomes  certainly  does  change  with 
different  periods  of  the  cell's  history  especially  within  the  rest- 
ing nucleus  and  yet  the  centers  of  chromosome  activity  may 
always  be  present  to  organize  the  chromatin  into  a  new  set  of 
elements  for  the  next  mitosis.  It  is  perhaps  difficult  to  believe 
that  the  chromatin  granules  (chromomeres)  find  their  way  back 
to  the  same  chromosome  with  the  prophase  of  each  mitosis  but 
the  existence  of  chromosome  centers  may  be  readily  conceived 
within  the  resting  nucleus  which  would  hold  the  number  of  chro- 
mosomes true  to  the  cell's  history. 

With  respect  to  the  nucleolus  there  is  abundant  evidence  that 
the  structure  is  not  a  permanent  organ  of  the  cell.  When  con- 
taining chromatin,  the  nucleolus  is  found  in  its  characteristic 
globular  state  only  during  the  resting  condition  of  the  nucleus. 
Its  chromatic  substance  passes  into  the  chromosomes  at  pro- 
phase  of  mitosis  and  the  nucleolus  generally  disappears  before 
metaphase.  Or  if  any  substance  is  left  after  the  chromosomes 
are  formed  the  remaining  structure  either  gradually  dissolves  or 
is  thrust  forth  bodily  into  the  cytoplasm  surrounding  the  mitotic 
figure  where  it  disappears  sooner  or  later.  The  nucleolus  in 
higher  types  of  mitosis  never  divides  to  pass  on  with  the  chro- 
mosomes to  the  daughter  nuclei,  but  such  a  history  is  reported 
in  the  yeast  cell.  If  the  nucleolus  has  any  function  in  heredity, 
as  has  been  claimed  (Dixon,  '99),  such  function  must  relate  to 
the  chromosomes  which  contribute  to  its  substance  or  derive 
material  from  it.  Besides  the  nucleoli  which  are  composed 
wholly  or  largely  of  chromatin,  there  are  also  those  which  seem 
to  have  little  if  any  relation  to  the  chromosomes.  Such  are 
well  known  in  the  spore  mother-cells  of  higher  plants  and  no 
investigator  has  been  able  to  connect  these  with  the  formation 
of  chromosomes  as  Wager  (:  04)  has  been  able  to  do  in  the  root 
tip.  It  was  upon  nucleoli  of  this  class  that  Strasburger  founded 
his  theory  that  the  structure  was  a  mass  of  reserve  material 
utilized  by  the  kinoplasm  during  mitosis  in  the  process  of  spindle 
formation.  Such  nucleoli  generally  fade  away  during  the  pro- 
phase  of  mitosis  and  either  entirely  disappear  or  the  remaining 
substance  is  thrust  out  into  the  cytoplasm  where  it  may  some- 


730  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

times   be  recognized  as  deeply  staining  globules  (the  so  called 
extranuclear  nucleoli). 

There  is  left  for  our  consideration  that  group  of  kinoplasmic 
structures  termed  centrosomes,  centrospheres,  and  blepharo- 
plasts  which,  when  accompanied  by  radiations,  are  called  asters. 
Some  authors  regard  these  structures  as  homologous  and  believe 
them  to  be  present  in  one  form  or  another  as  permanent  organs 
of  the  cell  in  certain  types  (see  discussion  of  Ikeno,  :O4). 
Against  this  view  stand  the  well  established  facts  of  an  increas- 
ing list  of  forms,  both  animals  and  plants,  in  which  these  struc- 
tures unquestionably  arise  de  novo  at  certain  periods  in  the  cell's 
history.  To  the  author  this  evidence  seems  insurmountable  and 
he  cannot  believe  that  the  aster  is  in  itself  a  permanent  organ 
of  the  cell.  We  shall  not  take  up  the  subjects  of  relationships 
here  for  such  discussions  have  proved  of  little  profit  except  in 
special  cases  where  the  various  types  of  structure  are  found  in 
closely  related  forms  or  in  the  same  life  history,  and  these  have 
scarcely  been  studied  at  all.  We  know  so  little  about  the  rela- 
tionships in  the  thallophytes,  where  relationships  must  be  sought 
if  present  at  all,  that  a  satisfactory  treatment  of  the  subject  is 
hardly  possible  at  present.  One  point  seems  to  have  escaped 
attention  in  the  writings  of  those  who  have  discussed  the  cen- 
trosome  problem.  The  active  elements  of  the  asters  are  not  the 
central  structures  (centrosomes,  centrospheres,  or  blepharoplasts) 
but  the  fibrillae  which  play  such  important  parts  as  spindle  fibers 
or  cilia.  This  fibrillar  condition  of  kinoplasm  has  a  fixed  place 
in  the  cycle  of  cell  division  appearing  with  each  mitosis  and  at 
the  time  of  cilia  formation,  but  the  fibrillae  are  not  permanent 
structures  of  the  cell.  There  is  some  evidence  that  the  centro- 
somes, centrospheres,  and  blepharoplasts  are  merely  regions  for 
the  development  and  attachment  of  these  fibrillae  and  as  such 
may  stand  as  the  morphological  expression  of  fibrillae-forming 
dynamic  centers  rather  than  as  organs  which  actually  induce  the 
development  of  fibrillae. 


No.  466.]          STUDIES   ON  PLANT  CELL.  — VIII.  731 

5.    THE    BALANCE    OF    NUCLEAR    AND    CYTOPLASMIC    ACTIVI- 
TIES IN  THE  PLANT  CELL. 

Two  regions  of  the  cell  are  sharply  distinguished  from  one 
another  with  respect  to  both  morphology  and  physiology.  They 
are  the  nucleus  and  the  cytoplasm.  The  nucleus  soon  dies  if 
isolated  from  cytoplasm  and  the  latter,  lacking  a  nucleus,  cannot 
be  kept  alive  indefinitely  unless  it  be  in  organic  connection  with 
a  nucleated  mass  of  protoplasm.  The  necessary  connection 
may  be  only  through  delicate  strands,  as  was  established  by 
Townsend  ('97),  and  also  seems  to  be  illustrated  in  the  instances 
of  intercellular  protoplasm  which  Michniewicz  (:  04)  reports  are 
connected  by  delicate  fibrillae  (plasmodesmen)  with  neighboring 
cells.  Some  very  interesting  adjustments  of  the  nucleus  and 
cytoplasm  to  one  another  have  been  reported  in  a  series  of 
investigations  of  Gerassimow  beginning  in  1890.  His  most 
recent  papers  of  the  past  year  (Gerassimow,  :  O4a,  :  O4b)  pre- 
sent a  general  summary  of  his  studies  and  constitute  a  very  im- 
portant contribution  to  the  subject.  They  will  furnish  much  of 
the  material  for  this  discussion. 

Gerassimow  has  found  that  the  cells  of  Spirogyra  and  other 
members  of  the  Conjugales  offer  admirable  material  for  the 
study  of  the  relations  between  the  nucleus  and  cytoplasm,  and 
throw  important  light  on  the  functions,  physiological  activities, 
and  interdependence  of  both  structures.  By  subjecting  fila- 
ments of  Spirogyra  during  cell  division  to  a  temperature  of 
o°  C.  or  treating  them  for  a  short  time  to  the  anaesthetic  influ- 
ence of  ether,  chloroform,  or  chloral  hydrate  it  is  possible  to 
arrest  the  processes  of  mitosis  at  different  stages  with  the  result 
that  the  protoplasm  may  become  variously  distributed  in  the 
daughter  cells,  (i)  A  daughter  cell  may  be  formed  lacking  a 
nucleus  but  containing  a  portion  of  the  divided  chromatophore 
in  a  peripheral  layer  of  cytoplasm.  (2)  A  single  cell  may  con- 
tain the  two  daughter  nuclei  either  separated  from  one  another 
or  more  or  less  intimately  associated  and  perhaps  wholly  fused 
depending  upon  how  far  the  processes  of  mitosis  have  pro- 
gressed before  the  cells  have  been  subjected  to  the  shock  of  the 


732  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

experiment.  (3)  Binucleate  cells  may  continue  their  growth 
with  subsequent  mitoses  which  when  treated  as  before  may  give 
daughter  cells  with  three  nuclei  and  one  nucleus  respectively  or 
with  two  each  or  indeed  a  cell  containing  four  nuclei.  Further- 
more these  nuclei  may  fuse  with  one  another  to  give  structures 
with  a  greatly  increased  chromatin  content.  (4)  In  place  of  the 
non-nucleated  cells  there  may  be  formed  chambers  containing 
cytoplasm  and  chromatophores,  but  without  nuclei,  which  remain 
in  open  communication  with  the  nucleated  companion  protoplast 
because  the  cell  wall  is  not  formed  entirely  across  the  mother- 
cell. 

Gerassimow  has  made  some  extended  observations  on  these 
various  types  of  cells,  and  presents  his  results  in  many  elaborate 
tables  and  diagrams.  We  can  only  give  an  outline  of  his  con- 
clusions, (i)  Cells  which  come  to  contain  unusually  large 
nuclei  through  the  suppression  of  mitosis  or  by  the  reuniting  of 
partially  divided  daughter  nuclei  increase  proportionally  in  size 
and  their  further  cell  division  is  postponed.  The  nuclei  of  such 
cells  have  of  course  the  peculiarity  of  an  increased  amount  of 
chromatin  content.  The  large  nuclei  may  later  fragment  into 
two  or  more  structures  which  separate  and  generally  come  to 
lie  at  a  distance  from  one  another  in  the  cytoplasm.  The  frag- 
ments finally  lose  their  powers  of  reproduction  and  exhibit 
marked  evidence  of  degeneration.  (2)  Cells  which  lack  nuclei 
may  form  starch  in.  the  usual  manner  in  the  presence  of  light 
and  exhibit  for  a  short  time  a  weaker  general  growth  than  nor- 
mal nucleated  cells.  The  power  to  develop  a  gelatinous  sheath 
also  becomes  markedly  weakened.  Finally  there  result  a  de- 
crease in  the  volume  of  the  cell,  a  fading  of  the  chromatophore, 
and  conditions  which  lead  to  eventual  death.  (3)  Chambers 
which  lack  nuclei  but  are  in  protoplasmic  union  with  nucleated 
cells  may  be  contrasted  sharply  with  the  non-nucleated  cells. 
They  exhibit  a  much  stronger  growth  for  a  longer  time  and  with 
a  greater  power  to  form  starch,  although  not  so  marked  as  in 
the  nucleated  cells,  and  the  chromatophores  retain  their  color. 
There  is  also  a  conspicuous  development  of  the  gelatinous 
sheath. 

Haberlandt,  Klebs,  Pfeffer,  Strasburger,  and  others  have  dis- 


No.  466.]  STUDIES   ON  PLANT  CELL.  —  VIII.  733 

cussed  the  relations  of  the  nucleus  to  the  surrounding  proto- 
plasm with  respect  to  both  dynamics  and  morphology.  Klebs 
('88)  indeed  anticipated  some  of  the  work  of  Gerassimow,  study- 
ing the  non-nucleated  cells  of  Zygnema  and  Spirogyra  and 
noting  the  ability  of  their  chromatophores  to  form  starch  in 
considerable  quantities  but  the  inability  of  the  protoplast  to  add 
to  the  cell  wall.  Klebs  was  able  to  keep  these  non-nucleated 
cells  alive  in  a  sugar  solution  for  from  four  to  six  weeks.  But 
for  the  most  part  the  discussions  of  the  balance  of  nuclear  and 
cytoplasmic  activities  in  the  plant  cell  have  been  very  general  in 
character. 

Some  principles  have  been,  however,  widely  held  for  several 
years  and  may  be  summarized.  The  necessity  of  the  nucleus  to 
the  life  of  the  cytoplasm  has  been  clearly  understood  but  the 
studies  of  Klebs  and  Gerassimow  indicate  that  the  nucleus  is  not 
directly  concerned  with  the  process  of  photosynthesis  which 
apparently  may  go  on  in  non-nucleated  cells  as  long  as  the  cyto- 
plasm retains  a  certain  degree  of  vitality.  A  non-nucleated  cell 
may  enlarge  slightly  but  it  is  not  probable  that  the  amount  of 
protoplasm  is  increased.  An  especially  interesting  feature  of 
non-nucleated  cells  is  the  inability  of  the  outer  plasma  membrane 
to  form  cellulose  walls  or  outer  membranes.  But  the  very  inter- 
esting studies  of  Townsend  ('97)  have  shown  that  this  power 
may  be  retained  provided  the  non-nucleated  mass  of  protoplasm 
is  connected  by  delicate  cytoplasmic  fibrils  with  a  nucleated 
mass.  It  thus  seems  clear  that  the  membrane-forming  possi- 
bilities of  the  outer  plasma  membrane  are  absolutely  dependent 
upon  dynamic  relations  with  the  nucleus.  While  the  chromato- 
phore  may  carry  on  the  processes  of  photosynthesis  independ- 
ently of  the  nucleus,  nevertheless  the  general  health  of  the  cell 
requires  the  activities  of  the  latter  so  that  the  nucleus  becomes 
necessary  to  any  extended  photosynthetic  work. 

It  has  frequently  been  stated  that  the  size  of  the  nucleus  is 
directly  proportionate  to  the  amount  of  cytoplasm  in  the  cell. 
There  are  many  favorable  illustrations  of  this  statement,  as  the 
extraordinarily  large  eggs  of  the  gymnosperms,  especially  the 
cycads,  whose  nuclei  are  by  far  the  largest  in  the  plant  kingdom. 
And  in  general  an  increase  in  the  amount  of  cytoplasm  is  accom- 


734  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

panied  either  by  a  marked  enlargement  of  the  nucleus  with  a 
corresponding  increase  in  the  chromatin  content  or  by  mitoses 
which  distribute  to  the  cytoplasm  a  greater  number  of  nuclei 
whose  sum  total  of  material  is  very  much  greater  than  before. 
Conversely  a  sudden  increase  in  nuclear  material  through  nuclear 
fusions  either  sexual  or  asexual  is  followed  almost  immediately 
by  general  cell  growth  and  increase  in  the  amount  of  cytoplasm. 
However,  such  fixed  growth  relations  between  nucleus  and  cyto- 
plasm can  hardly  be  an  established  physiological  law  for  certain 
highly  specialized  sperms  have  an  insignificant  amount  of  cyto- 
plasm proportionately  to  the  chromatin  that  is  contained  within 
the  gamete  nucleus.  It  is  evident  that  the  interrelations  of  the 
nucleus  and  the  cytoplasm  are  so  intimate  that  the  growth  activi- 
ties of  the  one  must  benefit  the  other,  but  that  this  principle 
can  be  formulated  in  definite  mathematical  ratios  seems  im- 
probable. 

The  dependence  of  the  nuclei  upon  favorable  situations  in  the 
cytoplasm  is  clearly  shown  in  cells. when  a  partial  or  general 
nuclear  degeneration  takes  place.  Thus  during  the  processes  of 
oogenesis  in  the  Peronosporales,  Saprolegniales,  and  in  Vau- 
cheria  there  is  present  a  period  when  the  most  of  the  numerous 
nuclei  within  the  oogonia  begin  to  break  down  and  finally 
become  disorganized.  The  causes  of  the  nuclear  degeneration 
are  not  entirely  clear  but  apparently  the  organ  is  unable  to 
supply  all  of  the  nuclei  in  their  respective  situations  in  the  cyto- 
plasm with  the  conditions  necessary  for  their  life.  There  is  con- 
sequently a  sort  of  struggle  for  existence  among  these  numerous 
nuclei  and  only  those  that  are  favorably  placed  in  the  cell  are 
able  to  survive.  In  all  forms  the  surviving  nuclei  occupy  a  situ- 
ation in  the  center  of  the  masses  of  protoplasm  which  are  to 
become  the  eggs  and  those  that  break  down  are  at  or  near  the 
periphery  of  the  cell.  In  several  genera  (e.g.,  Albugo,  Perono- 
spora,  Pythium,  Sclerospora,  Saprolegnia,  and  Achlya)  the  sur- 
viving nuclei  seem  to  owe  their  good  fortune  to  a  very  close 
association  with  the  cytoplasmic  structure  termed  the  coenocen- 
trum.  The  coenocentrum  is  a  clearly  differentiated  region  of 
the  cytoplasm  and  is  probably  the  morphological  expression  of  a 
dynamic  center  in  the  eggs  of  these  fungi.  Stevens'  ('99,  :  01) 


No.  466.]          STUDIES   ON  PLANT  CELL.— VIII.  735 

studies  on  Albugo  showed  that  the  coenocentra  exert  a  chemo- 
tactic  influence  upon  the  nuclei  in  their  vicinity,  drawing  them 
towards  the  mass  of  granular  material  in  this  favored  region  of 
the  cell,  and  it  is  clear  that  they  are  greatly  benefited  in  this 
situation  since  they  increase  in  size  while  the  nuclei  at  the 
periphery  break  done.  This  subject  is  discussed  in  detail  in  my 
paper  on  Saprolegnia  (Davis,  :  03,.  pp.  240-243)  a  form  which 
also  illustrates  exceptionally  well  the  same  principles  of  a  sur- 
vival of  certain  nuclei  among  many  which  degenerate,  because  of 
their  favorable  position  in  the  central  region  of  the  eggs  in  close 
proximity  to  coenocentra.  There  are  then  undoubtedly  regions 
of  the  cell  more  favorable  for  the  nutrition  of  nuclei  than  others 
and  the  positions  of  these  may  be  marked  by  morphological 
characters  as  illustrated  in  the  coenocentra.  That  similar  dyna- 
mic centers  may  also  be  present  when  there  is  little  morphologi- 
cal evidence  of  their  existence  is  indicated  in  the  processes  of 
oogenesis  in  Vaucheria  (Davis,  :  04)  which  exhibits  the  same 
principles  "of  extensive  nuclear  degeneration  as  are  found  in  the 
Peronosporales  and  Saprolegniales  and  the  survival  of  a  single 
nucleus  in  the  oogonium,  apparently  because  it  comes  to  lie  in  a 
mass  of  granular  cytoplasm  near  the  center  of  the  oogonium. 


736  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 


LITERATURE  CITED   IN  SECTION  VI,  "THE  PLANT  CELL." 

BARKER. 

:01.     A  Conjugating  Yeast.     Phil.   Trans.  Roy.  Soc.  London,  vol.  194, 

p.  467. 
BEER. 

:04.     The  Present  Position  of   Cell-wall  Research.      New  Phytologist, 

vol.  3,  p.  159. 
BOVERI. 

:  04.     Ergebnisse  iiber  die  Konstitution  der  chromatischen  Substanz  des 
Zellkerns.     Jena,  1904. 

BIJTSCHLI. 

'90.     Ueber  den  Bau  der  Bakterien  und  verwandter  Organismen.     Leip- 
zig, 1890. 
BUTSCHLI. 

'96.     Weitere  Ausfiihrungen  iiber  den  Bau  der  Cyanophyceen  und  Bak- 
terien.    Leipzig,  1896. 
BUTSCHLI. 

:02.     Bemerkungen    iiber  Cyanophyceen    und  Bakteriaceen.      Arch.  f. 

Protistenkunde,  vol.  i,  p.  41. 
CHAMBERLAIN. 

:03.     Mitoses  in  Pellia.     Bot.  Gaz.,  vol.  36,  p.  29. 
DAVIS. 

'98.     Kerntheilung  in  der  Tetrasporenmutterzelle  bei  Corallina  officinalis 
L.,  var.  mediterranea.     Ber.  d.  deut.  hot.  Gesellsch.,  vol.  16,  p.  266. 
DAVIS. 

'99.     The  Spore  Mother-cell  of  Anthoceros.     Bot.  Gaz.,  vol.  28,  p.  89. 
DAVIS. 

:  01.     Nuclear  Studies  on  Pellia.     Annals  of  Bot.,  vol.  15,  p.  147. 
DAVIS. 

:03.     Oogenesis  in  Saprolegnia.     Bot.  Gaz.,  vol.  35,  pp.  233,  320. 
DAVIS. 

:04.     Oogenesis  in  Vaucheria.     Bot.  Gaz.,  vol.  28,  p.  81. 
DIXON. 

'99.     The  Possible  Function  of    the  Nucleus  in  Heredity.     Annals  of 

Bot.,  vol.  8,  p.  269. 
FARMER  AND  MOORE. 

:  05.     On  the  Maiotic  Phase  (Reduction  Division)  in  Animals  and  Plants. 

Quart.  Jour.  After.  Set'.,  vol.  48,  p.  489. 
FARMER  AND  REEVES. 

'94.     On    the   Occurrence    of    Centrospheres  in  Pellia  epiphylla    Nees. 
Annals  of  Bot.,  vol.  8,  p.  219. 


No.  466.]          STUDIES  ON  PLANT  CELL.—  VIII.  737 

FEINBERG. 

:  00.     Ueber  den  Bau  der  Bakterien.     Centralb.  f.  Bak.,  pt.  i,  vol.  27, 

p.  417. 
FEINBERG. 

:  02.     Ueber  den  Bau  der  Hefezellen  und  iiber  ihre  Unterscheidung  von 
einzelligen  thierischen  Organismen.     Ber.  d.  deut.  hot.  Gesellsch., 
vol.  24,  p.  567. 
FISCHER. 

'97.     Untersuchungen  iiber  den  Bau  der  Cyanophyceen  und  Bakterien. 

Jena,  1897. 
FISCHER. 

'99.     Fixirung,  Farbung,  und  Bau  des  Protoplasmas.     Jena,  1899. 
GERASSIMOW. 

:  04a.     Zur  Physiologic  der  Zelle.     Bull.  Soc.  Imp.  Nat.  Moscou,  no.  I. 
GERASSIMOW. 

:04b.  Ueber  die  Grosse  des  Zellkerns.  Beih.  z.  Bot.  Centralb.,  vol.  18, 
P-45- 

GOLENKIN. 

'99.     Ueber   die  Befruchtung   bei  Sphceroplea   annulina  und  iiber  die 
Structur  der  Zellkerne  bei  einigen  griinen  Algen.     Bull.  Soc.  Imp. 
Nat.  Moscou,  p.  343. 
GREGOIRE  AND  BERGHS. 

:  O4.     La  figure  achromatique  dans  le  Pdlia  epiphylla.     La  Cellule,  vol. 

21,  p.  193. 
GREGOIRE  AND  WYGAERTS. 

:  03.  La  reconstitution  du  noyau  et  la  formation  des  chromosomes  dans 
les  cineses  somatiques.  i.  Racines  de  Trillium  grandiflorum  et 
telophase  homoeotypique  dans  Trillium  cernuum.  La  Cellule,  vol. 
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GUILLIERMOND. 

:03.     Recherches  cytologiques  sur  les  levures.     Rev.  Ge"n.  Bot.,  vol.  15, 

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GUILLIERMOND. 

:04.     Sur  le  noyau  de  la  levure.     Ann.  Mycol.,  vol.  2,  p.  184. 
HEGLER. 

:  01.  Untersuchungen  iiber  die  Organisation  der  Phycochromaceenzelle. 
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HlERONYMUS. 

'92.  Beitrage  zur  Morphologic  und  Biologic  der  Algen.  Cohrfs  Bettr. 
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HlRSHBRUCH. 

:02.     Die  Fortpflanzung  der  Hefezelle.     Centralb.  f.  Bak.,  pt.  2,  vol.  9, 

pp.  465,  513,  737. 
IKENO 
:  03.     Beitrage    zur    Kenntniss   der   pflanzlichen    Spermatogenese ;    die 


738  THE   AMERICAN  NATURALIST.       [VOL.  XXXIX. 

Spermatogenese    von    Marchantia  polymorpha.      Beth.   2.    Bot. 
Centralb.,  vol.   15,  p.  65. 
IKENO. 

:04.     Blepharoplasten  im  Pflanzenreich.     Biol.  Centralb.,  vol.  24,  p.  211. 
JANSSENS. 

:03.     A  propos  du  noyau  de  la  levure.     La  Cellule,  vol.  20,  p.  337. 
JANSSENS  AND  LEBLANC. 

'98.     Recherches  cytologiques  sur  la  cellule  de  levure.     La  Cellule,  vol. 

14,  p.  203. 
KOHL. 

:03.     Ueber  die  Organisation  und    Physiologic  der    Cyanophyceenzelle 

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KLEBS. 

'88.     Beitrage  zur  Physiologic  der  Pflanzenzelle.      Unters.  a.  d.  hot.  Inst. 

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LAWSON. 

:03.     On  the  Relationship  of  the  Nuclear  Membrane  to  the  Protoplast. 

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MACALLUM. 
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MANO. 
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Bakterien.     Centralb.  f.  Bak.,  pt.  2,  vol.  9,  p.  357- 
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:02.     Sur  le  protoplasme  des  Schizophytes.     Recueil  d.  rinst.  Bot.  Bru- 

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MERRIMAN. 

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MICHNIEWICZ. 

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MlGULA. 

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MOTTIER. 

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No.  466.]          STUDIES'  ON  PLANT  CELL.— VIII.  739 

NADSON. 

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sensch,  vol.  16. 


740  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

ZACHARIAS. 

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vol.  10,  p.  51. 


DIADASIA  PATTON;  A  GENUS  OF  BEES 

T.  D.  A.  COCKERELL. 

THE  genus  Diadasia  was  first  described  by  Patton  in  the 
Bulletin  of  the  United  States  Geological  Survey  (vol.  5,  p.  475). 
The  type  is  the  Melissodes  enavata  of  Cresson,  which,  as 
Patton  showed,  is  nearer  to  Anthophora  than  to  Melissodes. 
The  genus  occurs  in  our  southwestern  States,  and  is,  undoubt- 
edly, of  neotropical  derivation.  Ashmead  has  recently  placed 
it  as  a  synonym  of  the  South  American  Ancyloscelis  Latreille, 
but  it  appears  to  me  to  be  sufficiently  distinct. 

Our  species  of  Diadasia  have  not  hitherto  been  tabulated,  and 
as  I  have  now  seen*  all  the  species  but  one,  I  offer  tables  for 
their  identification.  The  species  of  Cresson  are  in  the  collec- 
tion at  the  Philadelphia  Academy  ;  I  have  been  permitted  to 
borrow  cotypes  from  that  institution,  through  Mr.  Viereck,  and 
this  has  enabled  me  to  clear  up  several  doubtful  points.  En- 
technia  toluca  (Melissodes  toluca  Cresson)  and  Dasiapis  ochracea 
Ckll.,  are  included  in  the  table,  as  the  first  has  for  some  years 
stood  in  our  lists  as  a  Diadasia,  while  the  latter  is  often  mis- 
taken for  a  species  of  that  genus. 

FEMALES. 

Hair  of  head  and  thorax  above  short  and  dense,  orange  fulvous  ;  abdomen 
with  four  clean  cut  bands  of  fulvous  tomentum  on  a  black  ground  ;  outer 
side  of  basal  joint  of  hind  tarsi  with  very  long,  strongly  plumose,  dark 
chocolate-colored  hairs  ;  inner  side  of  this  joint  with  shining  dark  ferru- 
ginous hair  ;  tegulae  red  ;  flagellunrall  dark;  front  rough  with  very  close 
punctures  .......  sumichrasti  (Cresson). 

Hair  of  thorax  not  thus  colored  ;  or  if  fulvous,  abdomen  not  thus  banded   i . 

1.  Scopa  on  outside  of  hind  legs  dark  gray  or  blackish  (in  afflicta  paler  on 
basal  part  of  tibiae.)  .  .          .          .         .         .         .         2. 

Scopa  on  outside  of  hind  legs  white,  or  not  gray  or  blackish  .         4. 

2.  Very  small  ;  less  than  8   mm.  long  ;  abdomen  with  narrow    bands  of 
tomentum  on    apical  margins  of  segments  ;  mesothorax  and   scutellum 

74i 


742  THE   AMERICAN  NATURALIST.        [VOL.  XXXIX. 

minutely,  extremely  densely  punctate  all  over,  therefore  rough  and  not 
shining  ......         Entechnia  toluca  (Cresson). 

Larger  ;  at  least  over  8  mm.  long  ;  mesothorax  well  punctured  but  shin- 
ing .  3. 

3.  Large  and  stout ;  about  12  mm.  long,  or  more 

D.  bituberculata  (Cresson). 
Smaller  ;  about  10  mm.  long,  or  less      .         .         .         afflicta  (Cresson). 

4.  Very  large  species,  about  15  mm.  long          .         megamorpha  Cockerell. 
Large  stout  species,  about  13  mm.  long  ;  hair  of  thorax  above  pchraceous 
or  fulvous,  with  the  disc  bare         ...         .         .         .         .         .         5. 

Smaller  species,  less  than  12  mm.  long  .         .         .         .         .         .         7. 

5.  Hind  spur  of  hind  tibia  straight  or  practically  so  ;  clypeus  more  closely 
punctured,  the  large  punctures  stronger         .         .         enavata  (Cresson). 
Hind  spur  of  hind  tibia  strongly  bent  at  end  ;  clypeus  less  closely  punc- 
tured, the  large  punctures  weaker  ....         .         .         .         6. 

6.  Legs  dark  red ;  abdominal   segments   3   and  4  with    a   narrow  apical 
fringe,  the  rest  thinly  hairy          ....         australis  (Cresson). 
Legs  black  ;  abdominal  segments  3  and  4  with  lateral  areas  where  the  sur- 
face is  raised  and  shining  black,  the  hair  on  it  being  very  sparse  and 
dark  .         .         .         .         .          .         australis  opuntia  (Cockerell). 

7.  Anterior  edge  of  abdominal  bands  curved,  the  basal  part  of  the  seg- 
ments  dark  ;    comparatively  large  and  broad  form  :  hind  spur   of  hind 
legs  curved  at  end       ....         australis  rinconis  (Cockerell). 
Anterior  edge  of  abdominal  bands  not  curved,  the  pubescence,  except  at 
margin,  uniformly  distributed  ;  smaller  forms  ....         8. 

8.  Hair  on  inner  side  of  basal  joint  of  hind  tarsi  light  ferruginous  ;  abdo- 
men entirely  covered  with  yellowish  tomentum       Dasiapis  ochracea  Ckll. 
Hair  on  inner  side  of  basal  joint  of  hind  tarsi  fuscous  or  black       .         9. 

9.  Face  broad,   eyes  scarcely  converging  below ;  eyes  narrow,  especially 
above  ;  mesothorax  shining,  impunctate  in  middle,   at  sides  with   large 
-scattered  punctures ;  abdomen  broad,   with  narrow  ochreous  hair-bands 
on  hind  margins  of  segments  2  to  4  ...         laticauda  Cockerell. 
Eyes  broader  and  shorter,  distinctly  converging  below  ;  mesothorax  dul- 
ler, the  sides  with  very  numerous  feeble  minute  punctures 

diniinuta  (Cresson). 

Larger  than  the  two  last  (i  I  mm.  long)  and  at  once  separated  from  them  by 
having  much  fuscous  or  black  hair  on  the  abdomen  ;  there  are  ochreous 
marginal  hair-bands  •  .  ...  .  friesei  Cockerell. 

MALES. 

Hair  of  face  black -nigrifrons  (Cresson). 

Hair  of  face  not  black     .........  i. 

I.    Apex   of   abdomen    truncate;    tongue  very   long;  maxillary   palpi   not 
fringed  with  hair  ;  size  very  small         .         .  Entechnia  toluca  (Cresson). 


No.  466.]  GENUS  DJ AD  ASIA.  743 

Apex  of  abdomen  bidentate          .         ...•'.         .         .         .  2. 

2.  Abdomen  above  with  much  black  hair  on  discs  of  segments  beyond  the 

second          .         .         .         .         .         .         .         .         .  — -g ^_        3. 

Abdomen  above  without  black  hair      .         . "       .         .         .         .  6. 

3.  Large;    at  least    13   mm.   long;  apical    teeth   of   abdomen   large   and 
divergent     .......  bituberculata  (Cresson). 

Smaller;  about  10  mm.  long;  apical  teeth  of  abdomen  small  and  close 
together        .         .  .'•'-.         .         .         .  •      .         .         .  4. 

4.  Hind  tibiae  thickened,  but  shape  not  remarkable  ;  basal  joint  of  hind 
tarsi  dark  ferruginous,  long,  slender,  and  curved,  its  apex  not  produced, 
the  hair  on  its  inner  side  orange  ;  maxillary  palpi  not  fringed  with  hair, 
except  a  little  tuft  at  the  end  of  second  joint ;  tegulae  light  rufous 

sumichrasti  (Cresson). 

Hind  tibiae  greatly  swollen,  narrowing  to  a  very  slender  base,  shaped 
something  like  a  wine-bottle  ;  basal  joint  of  hind  tarsi  dark,  not  so  long, 
with  black  or  dark  fuscous  hair  on  inner  side  •  .  .  .  .  5. 

5.  Tegulae  dark  but  decided  red  ;  second  submarginal  cell  much  narrowed 
above;  hair  of  mesothorax  white          .         .         .         .  afflicta  (Cresson). 
Tegulae  piceous  :  second  submarginal  cell  scarcely  narrowed  above  ;  hair 
of  mesothorax  and  scutellum  gray        .         .  afflicta  perafflicta  Cockerell. 

6.  Basal  joint  of  hind  tarsus  ending  in  a  long  process ;  species  covered 
with  gray  hair ;  maxillary  palpi  with  no  fringe  of  long  hairs,  but  second 
joint  ciliate  ...........  7. 

Basal  joint  of  hind  tarsus  not  ending  in  a  long  process          .         .  8. 

7.  Larger  forms      .......         australis  (Cresson). 

Smaller,  down  to  about  10  mm.  long    .         australis  rinconis  (Cockerell). 

8.  Very  large,  about  16  mm.  long  .         .         .  megamorpha  Cockerell. 
Rather  large,  length  over  10  mm.,  the  pubescence  more  or  less  ochrace- 
ous  on  thorax,  sometimes  quite  fulvous  ;    facial  quadrangle  longer  than 
broad  ............  9. 

Small,  length  less  than  10  mm.    .......          10. 

9.  Hair  of  thorax  more  or  less  fulvous    .         .         .  enavata  (Cresson). 
Hair  of  thorax  paler     ....          enavata  var.  densa  (Cresson). 

10.  Abdomen  above  shining  and  sparsely  hairy,  not  banded  ;  face  broad, 
orbits  little  converging  below  (distinctly  less  than  in  diminuta) 

nitidifrons  Cockerell . 
Abdomen  hairy,  the  hind  margins  of  the  segments  banded 

diminuta  (Cresson). 
Abdomen  covered  with  appressed  white  tomentum 

sphceralcearum  Cockerell. 

D.  albovestita  Provancher,  I  have  not  seen.  It  was  described 
from  the  female;  length  just  over  8  mm.,  flagellum  reddish 
beneath,  tegulae  brownish,  margins  of  abdominal  segments  pale 
yellow  and  covered  with  dense  whitish  pubescence  ;  apex  red- 


744  THE  AMERICAN  NATURALIST.       [VOL.  XXXIX. 

dish  brown.     It  must  be  similar  to  D.  sphceralcearnm,  but  the 
antennae  are  differently  colored. 

The  following  species  are  not  considered  valid  :  — 
D.  tricincta  Provancher,  from  California,  is  said  by  Fowler  to 
be  a  synonym  of  enavata.  This  cannot  be,  from  the  descrip- 
tion;  but  it  is  not  apparent  that  it  differs  from  afflicta.  D. 
nerea  Fowler,  from  California,  is  nigrifrons  Cresson  ;  D.  cinerea 
Fowler,  from  California,  is  bituberculata  Cresson.  Fowler  can 
hardly  be  blamed  for  describing  these  as  new,  as  when  he  pub- 
lished his  paper  Cresson's  species  were  supposed  to  belong  to 
Melissodes.  D.  ursina  (Cresson)  is  enavata.  D.  apacha  (Cres- 
son) is  diminuta.  The  types  of  apacJia  have  been  in  some 
liquid,  presumably  alcohol,  and  this  accounts  for  part  of  their 
characters.  I  formerly  separated  the  specimens  of  the  Middle 
Sonoran  zone  as  apacha,  leaving  those  of  the  Upper  Sonoran  as 
diminuta  ;  but  the  comparison  of  specimens  from  various  locali- 
ties appears  to  show  that  the  characters  relied  upon  are  too  vari- 
able to  serve  for  specific  distinction. 
Two  forms  are  new  :  — 

Diadasia  afflicta  (Cr.)  subsp.  perafflicta  n.  subsp. 

$  •  —  Tegulae  piceous  ;  second  submarginal  cell  scarcely  narrowed  above  ; 
hair  of  meso thorax  and  scutellum  gray. 

?  .  —  This  sex  does  not  materially  differ  from  true  afflicta. 

Hab. —  Clark  Co.,  Kansas,  1962  ft.,  May  (F.  H.  Snow,  1191)  ;  Hamilton 
Co.,  Kansas,  3350  ft.  (F.  H.  Snow,  460)  ;  Wallace  Co.,  Kansas,  3000  ft. 
(F.  H.  Snow,  852).  Three  females,  from  the  same  three  localities,  are 
numbered  851,  1197,  and  445. 

Diadasia  sphseralcearum  n.  sp. 

$. —  Length  7^  mm. ;  like  D.  diminuta  Cr.,  but  with  shorter,  perfectly 
white  pubescence,  and  a  narrower,  more  parallel-sided  abdomen ;  the 
pubescence  of  the  abdomen,  instead  of  being  loose  and  suberect  as  in  male 
diminuta,  is  appressed  (except  on  first  segment)  and  covers  the  surface  ; 
aside  from  the  pubescence,  the  hind  margins  of  the  segments  are  them- 
selves white ;  the  apex  is  bidentate,  the  teeth  being  like  those  of  diminuta, 
but  rather  larger ;  hind  legs  constructed  as  in  diminuta  ;  shining  hairless 
triangle  of  metathorax  much  smaller  than  in  diminuta  ;  posterior  part  of 
mesothorax  almost  nude  ;  tegulae  subhyaline,  ferruginous,  dark  at  base ; 
antennas  entirely  black. 


No.  466.]  GENUS  DI AD  ASIA.  745 

Hab. —  Between  Las  Cruces  and  Mesilla  Park,  New  Mexico,  at  flowers 
of  Sphceralcea  fendleri  lobata  (Wooton),  middle  of  August  (Cockerell).  It 
was  accompanied  by  Macroteropsis  latior  (Ckll.). 

The  distribution  of  the  species  in  States,  etc.,  so  far  as  known, 
is  as  follows :  — 

MEXICO. —  D.  diminuta  Cr. ;  sumichrasti  Cr.  ;  enavata  Cr.  (Lower  Cali- 
fornia). 

CALIFORNIA. —  D.  albovestita  Prov.  ;  afflicta  Cr.  (tricincta  Prov.) ;  nigri- 
frons  Cr.  ;  bituberculata  Cr.  ;  nitidifrons  Ckll.  ;  laticauda  Ckll. ;  friesei 
Ckll.  ;  enavata  Cr.  ;  diminuta  Cr.  (Palm  Spring,  Davidson}  ;  australis 
rinconis  Ckll. ;  australis  opuntice  Ckll. 

NEVADA. — D.  bituberculata  Cr. 

ARIZONA.  —  D.  diminuta  Cr.  (Bill  Williams'  Fork,  Snow,  Grand 
Canon,  Hopkins)  ;  australis  rinconis  Ckll.  (Bill  Williams'  Fork  and  Oak 
Creek  Canon,  Snow)  ;  enavata  Cr.  (Oak  Creek  Canon,  Snow). 

NEW  MEXICO. —  D.  diminuta  Cr.  ;  sphceralcearum  Ckll.  ;  australis  Cr. ; 
australis  rinconis  Ckll.  ;  enavata  Cr. ;  megamorpha  Ckll. 

TEXAS. —  D.  australis  rinconis  Ckll.  (part  of  Cresson's  original  austra- 
lis, as  shown  by  a  £  cotype)  ;  enavata  Cr. ;  enavata  v.  densa  Cr.  (a  color 
variation  merely)  ;  afflicta  Cr. 

KANSAS. — D.  australis  Cr.  (Wallace  Co.,  and  Morton  Co.,  Snow); 
enavata  Cr.  (Wallace  Co.,  Snow)  ;  diminuta  Cr.  (Hamilton  Co.,  Snow)  ; 
afflicta  perafflicta  Ckll. 

COLORADO. — -D.  enavata  Cr.  (Lamar,  Snow,  Palisade,  Gillette,  Jules- 
burg,  Ball,  Trinidad,  Titus)  ;  enavata  v.  densa  Cr.  (Rocky  Ford,  in  beet 
field,  P.  K.  Blinn)  ;  diminuta  Cr.  (Fort  Collins,  Trinidad,  Colo.  Agric. 
Coll)  ;  australis  Cr. 

D.  snmichrasti  Cr.,  is  peculiar  for  the  densely  punctured 
mesothorax,  but  the  blade  of  maxilla  is  broad  at  base  and  nar- 
row apically,  as  in  true  Diadasia.  The  maxillary  palpi  are  long, 
6-jointed.  The  sexes  do  not  look  much  alike,  but  close  com- 
parison confirms  their  identity. 

D.  australis  and  its  subspecies  may  be  found  visiting  the 
flowers  of  Opuntia.  The  small  species,  diminuta  and  its  allies, 
are  addicted  to  the  Malvaceae.  D.  megamorpha  (?)  was 
recorded  from  the  flowers  of  Sphceralcea  angustifolia,  but  the 
plant  was  really  6\  fendleri  lobata,  which  had  not  then  been 
differentiated. 

UNIVERSITY  OF  COLORADO, 
BOUI.DER,  COLORADO. 


